Ultrasound Microbubble Treatment Enhances Clathrin-Mediated Endocytosis and Fluid-Phase Uptake through Distinct Mechanisms
Drug delivery to tumors is limited by several factors, including drug permeability of the target cell plasma membrane. Ultrasound in combination with microbubbles (USMB) is a promising strategy to overcome these limitations. USMB treatment elicits enhanced cellular uptake of materials such as drugs,...
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| description | Drug delivery to tumors is limited by several factors, including drug permeability of the target cell plasma membrane. Ultrasound in combination with microbubbles (USMB) is a promising strategy to overcome these limitations. USMB treatment elicits enhanced cellular uptake of materials such as drugs, in part as a result of sheer stress and formation of transient membrane pores. Pores formed upon USMB treatment are rapidly resealed, suggesting that other processes such as enhanced endocytosis may contribute to the enhanced material uptake by cells upon USMB treatment. How USMB regulates endocytic processes remains incompletely understood. Cells constitutively utilize several distinct mechanisms of endocytosis, including clathrin-mediated endocytosis (CME) for the internalization of receptor-bound macromolecules such as Transferrin Receptor (TfR), and distinct mechanism(s) that mediate the majority of fluid-phase endocytosis. Tracking the abundance of TfR on the cell surface and the internalization of its ligand transferrin revealed that USMB acutely enhances the rate of CME. Total internal reflection fluorescence microscopy experiments revealed that USMB treatment altered the assembly of clathrin-coated pits, the basic structural units of CME. In addition, the rate of fluid-phase endocytosis was enhanced, but with delayed onset upon USMB treatment relative to the enhancement of CME, suggesting that the two processes are distinctly regulated by USMB. Indeed, vacuolin-1 or desipramine treatment prevented the enhancement of CME but not of fluid phase endocytosis upon USMB, suggesting that lysosome exocytosis and acid sphingomyelinase, respectively, are required for the regulation of CME but not fluid phase endocytosis upon USMB treatment. These results indicate that USMB enhances both CME and fluid phase endocytosis through distinct signaling mechanisms, and suggest that strategies for potentiating the enhancement of endocytosis upon USMB treatment may improve targeted drug delivery. |
| doi_str_mv | 10.1371/journal.pone.0156754 |
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Ultrasound in combination with microbubbles (USMB) is a promising strategy to overcome these limitations. USMB treatment elicits enhanced cellular uptake of materials such as drugs, in part as a result of sheer stress and formation of transient membrane pores. Pores formed upon USMB treatment are rapidly resealed, suggesting that other processes such as enhanced endocytosis may contribute to the enhanced material uptake by cells upon USMB treatment. How USMB regulates endocytic processes remains incompletely understood. Cells constitutively utilize several distinct mechanisms of endocytosis, including clathrin-mediated endocytosis (CME) for the internalization of receptor-bound macromolecules such as Transferrin Receptor (TfR), and distinct mechanism(s) that mediate the majority of fluid-phase endocytosis. Tracking the abundance of TfR on the cell surface and the internalization of its ligand transferrin revealed that USMB acutely enhances the rate of CME. Total internal reflection fluorescence microscopy experiments revealed that USMB treatment altered the assembly of clathrin-coated pits, the basic structural units of CME. In addition, the rate of fluid-phase endocytosis was enhanced, but with delayed onset upon USMB treatment relative to the enhancement of CME, suggesting that the two processes are distinctly regulated by USMB. Indeed, vacuolin-1 or desipramine treatment prevented the enhancement of CME but not of fluid phase endocytosis upon USMB, suggesting that lysosome exocytosis and acid sphingomyelinase, respectively, are required for the regulation of CME but not fluid phase endocytosis upon USMB treatment. These results indicate that USMB enhances both CME and fluid phase endocytosis through distinct signaling mechanisms, and suggest that strategies for potentiating the enhancement of endocytosis upon USMB treatment may improve targeted drug delivery.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0156754</identifier><identifier>PMID: 27275866</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Biology ; Biology and Life Sciences ; Cancer therapies ; Cell Line, Transformed ; Cell surface ; Clathrin ; Clathrin - metabolism ; Coated pits ; Desipramine ; Diagnostic ultrasonography ; Dosage and administration ; Drug delivery ; Drug delivery systems ; Drug Delivery Systems - methods ; Endocytosis ; Endocytosis - drug effects ; Exocytosis ; Exocytosis - drug effects ; Fluorescence ; Fluorescence microscopy ; Growth factors ; Heterocyclic Compounds, 4 or More Rings - metabolism ; Humans ; Internalization ; Kinases ; Lipids ; Lysosomes - metabolism ; Macromolecules ; Medicine and Health Sciences ; Membrane permeability ; Membranes ; Microbubbles ; Microscopy ; Pores ; Proteins ; Receptors, Transferrin - metabolism ; Science ; Sphingomyelin phosphodiesterase ; Studies ; Transferrin ; Tumors ; Ultrasonic imaging ; Ultrasonic Waves ; Ultrasound</subject><ispartof>PloS one, 2016-06, Vol.11 (6), p.e0156754-e0156754</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Fekri et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2016 Fekri et al 2016 Fekri et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c791t-e2aa9fb934d88d284007229abc380a88719d30e9e17c1bad680981b16a9550883</citedby><cites>FETCH-LOGICAL-c791t-e2aa9fb934d88d284007229abc380a88719d30e9e17c1bad680981b16a9550883</cites><orcidid>0000-0001-9192-6340</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4898768/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4898768/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27275866$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Johannes, Ludger</contributor><creatorcontrib>Fekri, Farnaz</creatorcontrib><creatorcontrib>Delos Santos, Ralph Christian</creatorcontrib><creatorcontrib>Karshafian, Raffi</creatorcontrib><creatorcontrib>Antonescu, Costin N</creatorcontrib><title>Ultrasound Microbubble Treatment Enhances Clathrin-Mediated Endocytosis and Fluid-Phase Uptake through Distinct Mechanisms</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Drug delivery to tumors is limited by several factors, including drug permeability of the target cell plasma membrane. 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Total internal reflection fluorescence microscopy experiments revealed that USMB treatment altered the assembly of clathrin-coated pits, the basic structural units of CME. In addition, the rate of fluid-phase endocytosis was enhanced, but with delayed onset upon USMB treatment relative to the enhancement of CME, suggesting that the two processes are distinctly regulated by USMB. Indeed, vacuolin-1 or desipramine treatment prevented the enhancement of CME but not of fluid phase endocytosis upon USMB, suggesting that lysosome exocytosis and acid sphingomyelinase, respectively, are required for the regulation of CME but not fluid phase endocytosis upon USMB treatment. These results indicate that USMB enhances both CME and fluid phase endocytosis through distinct signaling mechanisms, and suggest that strategies for potentiating the enhancement of endocytosis upon USMB treatment may improve targeted drug delivery.</description><subject>Analysis</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Cancer therapies</subject><subject>Cell Line, Transformed</subject><subject>Cell surface</subject><subject>Clathrin</subject><subject>Clathrin - metabolism</subject><subject>Coated pits</subject><subject>Desipramine</subject><subject>Diagnostic ultrasonography</subject><subject>Dosage and administration</subject><subject>Drug delivery</subject><subject>Drug delivery systems</subject><subject>Drug Delivery Systems - methods</subject><subject>Endocytosis</subject><subject>Endocytosis - drug effects</subject><subject>Exocytosis</subject><subject>Exocytosis - drug effects</subject><subject>Fluorescence</subject><subject>Fluorescence microscopy</subject><subject>Growth factors</subject><subject>Heterocyclic Compounds, 4 or More Rings - metabolism</subject><subject>Humans</subject><subject>Internalization</subject><subject>Kinases</subject><subject>Lipids</subject><subject>Lysosomes - metabolism</subject><subject>Macromolecules</subject><subject>Medicine and Health Sciences</subject><subject>Membrane permeability</subject><subject>Membranes</subject><subject>Microbubbles</subject><subject>Microscopy</subject><subject>Pores</subject><subject>Proteins</subject><subject>Receptors, Transferrin - metabolism</subject><subject>Science</subject><subject>Sphingomyelin phosphodiesterase</subject><subject>Studies</subject><subject>Transferrin</subject><subject>Tumors</subject><subject>Ultrasonic imaging</subject><subject>Ultrasonic Waves</subject><subject>Ultrasound</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk19v0zAUxSMEYqPwDRBEQkLw0GI7f2y_TJrKBpVWDcHKq3VjO42HG5fYQYxPj0O7qUGTQHmIZf_O8fWxb5I8x2iGM4rfXbu-a8HOtq7VM4SLkhb5g-QY84xMS4Kyhwfjo-SJ99cIFRkry8fJEaGEFnF4nPxa2dCBd32r0qWRnav6qrI6veo0hI1uQ3rWNtBK7dO5hdB0pp0utTIQtIpLysmb4LzxKUSDc9sbNf3UgNfpahvgm06jwvXrJn1vfDCtDOlSy-hn_MY_TR7VYL1-tv9PktX52dX84_Ti8sNifnoxlZTjMNUEgNcVz3LFmCIsR4gSwqGSGUPAGMVcZUhzjanEFaiSIc5whUvgRYEYyybJy53v1jov9rF5gSnPGclzMhCLHaEcXIttZzbQ3QgHRvyZcN1aQBeMtFrUjOESlQojUuaQUQ60zpTEZdyRFjHgSXKy362vNlrJGGEHdmQ6XmlNI9buh8gZZ7QcinmzN-jc9177IDbGS20ttNr1sW6GGCWcYPpvlPIispQPrq_-Qu8PYk-tIZ7VtLWLJcrBVJzmRV6UhGEUqdk9VPyU3hgZn2Nt4vxI8HYkiEzQP8Maeu_F4svn_2cvv47Z1wdso8GGxjvbB-NaPwbzHRgfuPedru_uAyMxdNNtGmLoJrHvpih7cXiXd6Lb9sl-AxyvGYY</recordid><startdate>20160608</startdate><enddate>20160608</enddate><creator>Fekri, Farnaz</creator><creator>Delos Santos, Ralph Christian</creator><creator>Karshafian, Raffi</creator><creator>Antonescu, Costin N</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-9192-6340</orcidid></search><sort><creationdate>20160608</creationdate><title>Ultrasound Microbubble Treatment Enhances Clathrin-Mediated Endocytosis and Fluid-Phase Uptake through Distinct Mechanisms</title><author>Fekri, Farnaz ; Delos Santos, Ralph Christian ; Karshafian, Raffi ; Antonescu, Costin N</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c791t-e2aa9fb934d88d284007229abc380a88719d30e9e17c1bad680981b16a9550883</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Analysis</topic><topic>Biology</topic><topic>Biology and Life Sciences</topic><topic>Cancer therapies</topic><topic>Cell Line, Transformed</topic><topic>Cell surface</topic><topic>Clathrin</topic><topic>Clathrin - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fekri, Farnaz</au><au>Delos Santos, Ralph Christian</au><au>Karshafian, Raffi</au><au>Antonescu, Costin N</au><au>Johannes, Ludger</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ultrasound Microbubble Treatment Enhances Clathrin-Mediated Endocytosis and Fluid-Phase Uptake through Distinct Mechanisms</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-06-08</date><risdate>2016</risdate><volume>11</volume><issue>6</issue><spage>e0156754</spage><epage>e0156754</epage><pages>e0156754-e0156754</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Drug delivery to tumors is limited by several factors, including drug permeability of the target cell plasma membrane. Ultrasound in combination with microbubbles (USMB) is a promising strategy to overcome these limitations. USMB treatment elicits enhanced cellular uptake of materials such as drugs, in part as a result of sheer stress and formation of transient membrane pores. Pores formed upon USMB treatment are rapidly resealed, suggesting that other processes such as enhanced endocytosis may contribute to the enhanced material uptake by cells upon USMB treatment. How USMB regulates endocytic processes remains incompletely understood. Cells constitutively utilize several distinct mechanisms of endocytosis, including clathrin-mediated endocytosis (CME) for the internalization of receptor-bound macromolecules such as Transferrin Receptor (TfR), and distinct mechanism(s) that mediate the majority of fluid-phase endocytosis. Tracking the abundance of TfR on the cell surface and the internalization of its ligand transferrin revealed that USMB acutely enhances the rate of CME. Total internal reflection fluorescence microscopy experiments revealed that USMB treatment altered the assembly of clathrin-coated pits, the basic structural units of CME. In addition, the rate of fluid-phase endocytosis was enhanced, but with delayed onset upon USMB treatment relative to the enhancement of CME, suggesting that the two processes are distinctly regulated by USMB. Indeed, vacuolin-1 or desipramine treatment prevented the enhancement of CME but not of fluid phase endocytosis upon USMB, suggesting that lysosome exocytosis and acid sphingomyelinase, respectively, are required for the regulation of CME but not fluid phase endocytosis upon USMB treatment. These results indicate that USMB enhances both CME and fluid phase endocytosis through distinct signaling mechanisms, and suggest that strategies for potentiating the enhancement of endocytosis upon USMB treatment may improve targeted drug delivery.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27275866</pmid><doi>10.1371/journal.pone.0156754</doi><orcidid>https://orcid.org/0000-0001-9192-6340</orcidid><oa>free_for_read</oa></addata></record> |
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| issn | 1932-6203 1932-6203 |
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| subjects | Analysis Biology Biology and Life Sciences Cancer therapies Cell Line, Transformed Cell surface Clathrin Clathrin - metabolism Coated pits Desipramine Diagnostic ultrasonography Dosage and administration Drug delivery Drug delivery systems Drug Delivery Systems - methods Endocytosis Endocytosis - drug effects Exocytosis Exocytosis - drug effects Fluorescence Fluorescence microscopy Growth factors Heterocyclic Compounds, 4 or More Rings - metabolism Humans Internalization Kinases Lipids Lysosomes - metabolism Macromolecules Medicine and Health Sciences Membrane permeability Membranes Microbubbles Microscopy Pores Proteins Receptors, Transferrin - metabolism Science Sphingomyelin phosphodiesterase Studies Transferrin Tumors Ultrasonic imaging Ultrasonic Waves Ultrasound |
| title | Ultrasound Microbubble Treatment Enhances Clathrin-Mediated Endocytosis and Fluid-Phase Uptake through Distinct Mechanisms |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-31T12%3A59%3A55IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Ultrasound%20Microbubble%20Treatment%20Enhances%20Clathrin-Mediated%20Endocytosis%20and%20Fluid-Phase%20Uptake%20through%20Distinct%20Mechanisms&rft.jtitle=PloS%20one&rft.au=Fekri,%20Farnaz&rft.date=2016-06-08&rft.volume=11&rft.issue=6&rft.spage=e0156754&rft.epage=e0156754&rft.pages=e0156754-e0156754&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0156754&rft_dat=%3Cgale_plos_%3EA454562810%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1794824428&rft_id=info:pmid/27275866&rft_galeid=A454562810&rft_doaj_id=oai_doaj_org_article_f881606d10264a379a7f3dc161b17505&rfr_iscdi=true |