Dynamic Biodistribution of Extracellular Vesicles in Vivo Using a Multimodal Imaging Reporter

Extracellular vesicles (EVs) are nanosized vesicles released by normal and diseased cells as a novel form of intercellular communication and can serve as an effective therapeutic vehicle for genes and drugs. Yet, much remains unknown about the in vivo properties of EVs such as tissue distribution, b...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:ACS nano 2014-01, Vol.8 (1), p.483-494
Hauptverfasser: Lai, Charles P, Mardini, Osama, Ericsson, Maria, Prabhakar, Shilpa, Maguire, Casey A, Chen, John W, Tannous, Bakhos A, Breakefield, Xandra O
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 494
container_issue 1
container_start_page 483
container_title ACS nano
container_volume 8
creator Lai, Charles P
Mardini, Osama
Ericsson, Maria
Prabhakar, Shilpa
Maguire, Casey A
Chen, John W
Tannous, Bakhos A
Breakefield, Xandra O
description Extracellular vesicles (EVs) are nanosized vesicles released by normal and diseased cells as a novel form of intercellular communication and can serve as an effective therapeutic vehicle for genes and drugs. Yet, much remains unknown about the in vivo properties of EVs such as tissue distribution, blood levels, and urine clearance, important parameters that will define their therapeutic effectiveness and potential toxicity. Here we combined Gaussia luciferase and metabolic biotinylation to create a sensitive EV reporter (EV-GlucB) for multimodal imaging in vivo, as well as monitoring of EV levels in the organs and biofluids ex vivo after administration of EVs. Bioluminescence and fluorescence-mediated tomography imaging on mice displayed a predominant localization of intravenously administered EVs in the spleen followed by the liver. Monitoring EV signal in the organs, blood, and urine further revealed that the EVs first undergo a rapid distribution phase followed by a longer elimination phase via hepatic and renal routes within six hours, which are both faster than previously reported using dye-labeled EVs. Moreover, we demonstrate systemically injected EVs can be delivered to tumor sites within an hour following injection. Altogether, we show the EVs are dynamically processed in vivo with accurate spatiotemporal resolution and target a number of normal organs as well as tumors with implications for disease pathology and therapeutic design.
doi_str_mv 10.1021/nn404945r
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_3934350</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1762055816</sourcerecordid><originalsourceid>FETCH-LOGICAL-a471t-c62bcdcd44da663c1a9323f4449293fd866b5f240fd56962fb724a4a534f87d13</originalsourceid><addsrcrecordid>eNptkclKBDEQhoMo7gdfQHIR9DCavbsvgruCIoiKFwnpLGOkOxmTbtG3t4fRQcFTFVUff_1VBcAWRvsYEXwQAkOsYjwtgFVcUTFCpXhanOccr4C1nF8R4kVZiGWwQhgtKcflKng-_Qyq9Roe-2h87pKv-87HAKODZx9dUto2Td-oBB9t9rqxGfoAH_17hA_ZhzFU8KZvOt9Goxp41arxtHhnJzF1Nm2AJaeabDe_4zp4OD-7P7kcXd9eXJ0cXY8UK3A30oLU2mjDmFFCUI1VRQl1jLGKVNSZUoiaO8KQM1xUgri6IEwxxSlzZWEwXQeHM91JX7fWaBsG542cJN-q9Cmj8vJvJ_gXOY7vklaUUY4Ggd1vgRTfeps72fo8XV0FG_sscSEI4rzEYkD3ZqhOMedk3XwMRnL6Djl_x8Bu__Y1J3_uPwA7M0DpLF9jn8Jwpn-EvgBDr5Nx</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1762055816</pqid></control><display><type>article</type><title>Dynamic Biodistribution of Extracellular Vesicles in Vivo Using a Multimodal Imaging Reporter</title><source>ACS Publications</source><source>MEDLINE</source><creator>Lai, Charles P ; Mardini, Osama ; Ericsson, Maria ; Prabhakar, Shilpa ; Maguire, Casey A ; Chen, John W ; Tannous, Bakhos A ; Breakefield, Xandra O</creator><creatorcontrib>Lai, Charles P ; Mardini, Osama ; Ericsson, Maria ; Prabhakar, Shilpa ; Maguire, Casey A ; Chen, John W ; Tannous, Bakhos A ; Breakefield, Xandra O</creatorcontrib><description>Extracellular vesicles (EVs) are nanosized vesicles released by normal and diseased cells as a novel form of intercellular communication and can serve as an effective therapeutic vehicle for genes and drugs. Yet, much remains unknown about the in vivo properties of EVs such as tissue distribution, blood levels, and urine clearance, important parameters that will define their therapeutic effectiveness and potential toxicity. Here we combined Gaussia luciferase and metabolic biotinylation to create a sensitive EV reporter (EV-GlucB) for multimodal imaging in vivo, as well as monitoring of EV levels in the organs and biofluids ex vivo after administration of EVs. Bioluminescence and fluorescence-mediated tomography imaging on mice displayed a predominant localization of intravenously administered EVs in the spleen followed by the liver. Monitoring EV signal in the organs, blood, and urine further revealed that the EVs first undergo a rapid distribution phase followed by a longer elimination phase via hepatic and renal routes within six hours, which are both faster than previously reported using dye-labeled EVs. Moreover, we demonstrate systemically injected EVs can be delivered to tumor sites within an hour following injection. Altogether, we show the EVs are dynamically processed in vivo with accurate spatiotemporal resolution and target a number of normal organs as well as tumors with implications for disease pathology and therapeutic design.</description><identifier>ISSN: 1936-0851</identifier><identifier>EISSN: 1936-086X</identifier><identifier>DOI: 10.1021/nn404945r</identifier><identifier>PMID: 24383518</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Animals ; Biocompatibility ; Biomedical materials ; Genes, Reporter ; Genetic Vectors ; HEK293 Cells ; Humans ; Imaging ; In vivo testing ; In vivo tests ; Mice ; Microscopy, Electron, Transmission ; Multimodal Imaging ; Nanostructure ; Organs ; Surgical implants ; Tissue Distribution ; Vesicles</subject><ispartof>ACS nano, 2014-01, Vol.8 (1), p.483-494</ispartof><rights>Copyright © 2014 American Chemical Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a471t-c62bcdcd44da663c1a9323f4449293fd866b5f240fd56962fb724a4a534f87d13</citedby><cites>FETCH-LOGICAL-a471t-c62bcdcd44da663c1a9323f4449293fd866b5f240fd56962fb724a4a534f87d13</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/nn404945r$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/nn404945r$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>230,314,776,780,881,2752,27053,27901,27902,56713,56763</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24383518$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lai, Charles P</creatorcontrib><creatorcontrib>Mardini, Osama</creatorcontrib><creatorcontrib>Ericsson, Maria</creatorcontrib><creatorcontrib>Prabhakar, Shilpa</creatorcontrib><creatorcontrib>Maguire, Casey A</creatorcontrib><creatorcontrib>Chen, John W</creatorcontrib><creatorcontrib>Tannous, Bakhos A</creatorcontrib><creatorcontrib>Breakefield, Xandra O</creatorcontrib><title>Dynamic Biodistribution of Extracellular Vesicles in Vivo Using a Multimodal Imaging Reporter</title><title>ACS nano</title><addtitle>ACS Nano</addtitle><description>Extracellular vesicles (EVs) are nanosized vesicles released by normal and diseased cells as a novel form of intercellular communication and can serve as an effective therapeutic vehicle for genes and drugs. Yet, much remains unknown about the in vivo properties of EVs such as tissue distribution, blood levels, and urine clearance, important parameters that will define their therapeutic effectiveness and potential toxicity. Here we combined Gaussia luciferase and metabolic biotinylation to create a sensitive EV reporter (EV-GlucB) for multimodal imaging in vivo, as well as monitoring of EV levels in the organs and biofluids ex vivo after administration of EVs. Bioluminescence and fluorescence-mediated tomography imaging on mice displayed a predominant localization of intravenously administered EVs in the spleen followed by the liver. Monitoring EV signal in the organs, blood, and urine further revealed that the EVs first undergo a rapid distribution phase followed by a longer elimination phase via hepatic and renal routes within six hours, which are both faster than previously reported using dye-labeled EVs. Moreover, we demonstrate systemically injected EVs can be delivered to tumor sites within an hour following injection. Altogether, we show the EVs are dynamically processed in vivo with accurate spatiotemporal resolution and target a number of normal organs as well as tumors with implications for disease pathology and therapeutic design.</description><subject>Animals</subject><subject>Biocompatibility</subject><subject>Biomedical materials</subject><subject>Genes, Reporter</subject><subject>Genetic Vectors</subject><subject>HEK293 Cells</subject><subject>Humans</subject><subject>Imaging</subject><subject>In vivo testing</subject><subject>In vivo tests</subject><subject>Mice</subject><subject>Microscopy, Electron, Transmission</subject><subject>Multimodal Imaging</subject><subject>Nanostructure</subject><subject>Organs</subject><subject>Surgical implants</subject><subject>Tissue Distribution</subject><subject>Vesicles</subject><issn>1936-0851</issn><issn>1936-086X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNptkclKBDEQhoMo7gdfQHIR9DCavbsvgruCIoiKFwnpLGOkOxmTbtG3t4fRQcFTFVUff_1VBcAWRvsYEXwQAkOsYjwtgFVcUTFCpXhanOccr4C1nF8R4kVZiGWwQhgtKcflKng-_Qyq9Roe-2h87pKv-87HAKODZx9dUto2Td-oBB9t9rqxGfoAH_17hA_ZhzFU8KZvOt9Goxp41arxtHhnJzF1Nm2AJaeabDe_4zp4OD-7P7kcXd9eXJ0cXY8UK3A30oLU2mjDmFFCUI1VRQl1jLGKVNSZUoiaO8KQM1xUgri6IEwxxSlzZWEwXQeHM91JX7fWaBsG542cJN-q9Cmj8vJvJ_gXOY7vklaUUY4Ggd1vgRTfeps72fo8XV0FG_sscSEI4rzEYkD3ZqhOMedk3XwMRnL6Djl_x8Bu__Y1J3_uPwA7M0DpLF9jn8Jwpn-EvgBDr5Nx</recordid><startdate>20140128</startdate><enddate>20140128</enddate><creator>Lai, Charles P</creator><creator>Mardini, Osama</creator><creator>Ericsson, Maria</creator><creator>Prabhakar, Shilpa</creator><creator>Maguire, Casey A</creator><creator>Chen, John W</creator><creator>Tannous, Bakhos A</creator><creator>Breakefield, Xandra O</creator><general>American Chemical Society</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>7SR</scope><scope>7U5</scope><scope>8BQ</scope><scope>8FD</scope><scope>JG9</scope><scope>L7M</scope><scope>5PM</scope></search><sort><creationdate>20140128</creationdate><title>Dynamic Biodistribution of Extracellular Vesicles in Vivo Using a Multimodal Imaging Reporter</title><author>Lai, Charles P ; Mardini, Osama ; Ericsson, Maria ; Prabhakar, Shilpa ; Maguire, Casey A ; Chen, John W ; Tannous, Bakhos A ; Breakefield, Xandra O</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a471t-c62bcdcd44da663c1a9323f4449293fd866b5f240fd56962fb724a4a534f87d13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Biocompatibility</topic><topic>Biomedical materials</topic><topic>Genes, Reporter</topic><topic>Genetic Vectors</topic><topic>HEK293 Cells</topic><topic>Humans</topic><topic>Imaging</topic><topic>In vivo testing</topic><topic>In vivo tests</topic><topic>Mice</topic><topic>Microscopy, Electron, Transmission</topic><topic>Multimodal Imaging</topic><topic>Nanostructure</topic><topic>Organs</topic><topic>Surgical implants</topic><topic>Tissue Distribution</topic><topic>Vesicles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lai, Charles P</creatorcontrib><creatorcontrib>Mardini, Osama</creatorcontrib><creatorcontrib>Ericsson, Maria</creatorcontrib><creatorcontrib>Prabhakar, Shilpa</creatorcontrib><creatorcontrib>Maguire, Casey A</creatorcontrib><creatorcontrib>Chen, John W</creatorcontrib><creatorcontrib>Tannous, Bakhos A</creatorcontrib><creatorcontrib>Breakefield, Xandra O</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Engineered Materials Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Materials Research Database</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>ACS nano</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lai, Charles P</au><au>Mardini, Osama</au><au>Ericsson, Maria</au><au>Prabhakar, Shilpa</au><au>Maguire, Casey A</au><au>Chen, John W</au><au>Tannous, Bakhos A</au><au>Breakefield, Xandra O</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dynamic Biodistribution of Extracellular Vesicles in Vivo Using a Multimodal Imaging Reporter</atitle><jtitle>ACS nano</jtitle><addtitle>ACS Nano</addtitle><date>2014-01-28</date><risdate>2014</risdate><volume>8</volume><issue>1</issue><spage>483</spage><epage>494</epage><pages>483-494</pages><issn>1936-0851</issn><eissn>1936-086X</eissn><abstract>Extracellular vesicles (EVs) are nanosized vesicles released by normal and diseased cells as a novel form of intercellular communication and can serve as an effective therapeutic vehicle for genes and drugs. Yet, much remains unknown about the in vivo properties of EVs such as tissue distribution, blood levels, and urine clearance, important parameters that will define their therapeutic effectiveness and potential toxicity. Here we combined Gaussia luciferase and metabolic biotinylation to create a sensitive EV reporter (EV-GlucB) for multimodal imaging in vivo, as well as monitoring of EV levels in the organs and biofluids ex vivo after administration of EVs. Bioluminescence and fluorescence-mediated tomography imaging on mice displayed a predominant localization of intravenously administered EVs in the spleen followed by the liver. Monitoring EV signal in the organs, blood, and urine further revealed that the EVs first undergo a rapid distribution phase followed by a longer elimination phase via hepatic and renal routes within six hours, which are both faster than previously reported using dye-labeled EVs. Moreover, we demonstrate systemically injected EVs can be delivered to tumor sites within an hour following injection. Altogether, we show the EVs are dynamically processed in vivo with accurate spatiotemporal resolution and target a number of normal organs as well as tumors with implications for disease pathology and therapeutic design.</abstract><cop>United States</cop><pub>American Chemical Society</pub><pmid>24383518</pmid><doi>10.1021/nn404945r</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1936-0851
ispartof ACS nano, 2014-01, Vol.8 (1), p.483-494
issn 1936-0851
1936-086X
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_3934350
source ACS Publications; MEDLINE
subjects Animals
Biocompatibility
Biomedical materials
Genes, Reporter
Genetic Vectors
HEK293 Cells
Humans
Imaging
In vivo testing
In vivo tests
Mice
Microscopy, Electron, Transmission
Multimodal Imaging
Nanostructure
Organs
Surgical implants
Tissue Distribution
Vesicles
title Dynamic Biodistribution of Extracellular Vesicles in Vivo Using a Multimodal Imaging Reporter
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-31T11%3A37%3A53IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Dynamic%20Biodistribution%20of%20Extracellular%20Vesicles%20in%20Vivo%20Using%20a%20Multimodal%20Imaging%20Reporter&rft.jtitle=ACS%20nano&rft.au=Lai,%20Charles%20P&rft.date=2014-01-28&rft.volume=8&rft.issue=1&rft.spage=483&rft.epage=494&rft.pages=483-494&rft.issn=1936-0851&rft.eissn=1936-086X&rft_id=info:doi/10.1021/nn404945r&rft_dat=%3Cproquest_pubme%3E1762055816%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1762055816&rft_id=info:pmid/24383518&rfr_iscdi=true