Endosomal signalling via exosome surface TGFβ-1
Identifieur interne : 000783 ( Pmc/Checkpoint ); précédent : 000782; suivant : 000784Endosomal signalling via exosome surface TGFβ-1
Auteurs : Ganesh Vilas Shelke [Suède] ; Yanan Yin [Suède, République populaire de Chine] ; Su Chul Jang [Suède] ; Cecilia L Sser [Suède] ; Stefan Wennmalm [Suède] ; Hans Jürgen Hoffmann [Danemark] ; Li Li [République populaire de Chine] ; Yong Song Gho [Corée du Sud] ; Jonas Andreas Nilsson [Suède] ; Jan Lötvall [Suède]Source :
- Journal of Extracellular Vesicles [ 2001-3078 ] ; 2019.
Abstract
Extracellular vesicles such as exosomes convey biological messages between cells, either by surface-to-surface interaction or by shuttling of bioactive molecules to a recipient cell’s cytoplasm. Here we show that exosomes released by mast cells harbour both active and latent transforming growth factor β-1 (TGFβ-1) on their surfaces. The latent form of TGFβ-1 is associated with the exosomes via heparinase-II and pH-sensitive elements. These vesicles traffic to the endocytic compartment of recipient human mesenchymal stem cells (MSCs) within 60 min of exposure. Further, the exosomes-associated TGFβ-1 is retained within the endosomal compartments at the time of signalling, which results in prolonged cellular signalling compared to free-TGFβ-1. These exosomes induce a migratory phenotype in primary MSCs involving SMAD-dependent pathways. Our results show that mast cell-derived exosomes are decorated with latent TGFβ-1 and are retained in recipient MSC endosomes, influencing recipient cell migratory phenotype. We conclude that exosomes can convey signalling within endosomes by delivering bioactive surface ligands to this intracellular compartment.
Url:
DOI: 10.1080/20013078.2019.1650458
PubMed: 31595182
PubMed Central: 6764367
Affiliations:
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<front><div type="abstract" xml:lang="en"><title>ABSTRACT</title>
<p>Extracellular vesicles such as exosomes convey biological messages between cells, either by surface-to-surface interaction or by shuttling of bioactive molecules to a recipient cell’s cytoplasm. Here we show that exosomes released by mast cells harbour both active and latent transforming growth factor β-1 (TGFβ-1) on their surfaces. The latent form of TGFβ-1 is associated with the exosomes via heparinase-II and pH-sensitive elements. These vesicles traffic to the endocytic compartment of recipient human mesenchymal stem cells (MSCs) within 60 min of exposure. Further, the exosomes-associated TGFβ-1 is retained within the endosomal compartments at the time of signalling, which results in prolonged cellular signalling compared to free-TGFβ-1. These exosomes induce a migratory phenotype in primary MSCs involving SMAD-dependent pathways. Our results show that mast cell-derived exosomes are decorated with latent TGFβ-1 and are retained in recipient MSC endosomes, influencing recipient cell migratory phenotype. We conclude that exosomes can convey signalling within endosomes by delivering bioactive surface ligands to this intracellular compartment.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Extracell Vesicles</journal-id>
<journal-id journal-id-type="iso-abbrev">J Extracell Vesicles</journal-id>
<journal-id journal-id-type="publisher-id">ZJEV</journal-id>
<journal-id journal-id-type="publisher-id">zjev20</journal-id>
<journal-title-group><journal-title>Journal of Extracellular Vesicles</journal-title>
</journal-title-group>
<issn pub-type="epub">2001-3078</issn>
<publisher><publisher-name>Taylor & Francis</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31595182</article-id>
<article-id pub-id-type="pmc">6764367</article-id>
<article-id pub-id-type="publisher-id">1650458</article-id>
<article-id pub-id-type="doi">10.1080/20013078.2019.1650458</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Endosomal signalling via exosome surface TGFβ-1</article-title>
<alt-title alt-title-type="running-authors">G. V. SHELKE ET AL.</alt-title>
<alt-title alt-title-type="running-title">JOURNAL OF EXTRACELLULAR VESICLES</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0001-5883-8082</contrib-id>
<name><surname>Shelke</surname>
<given-names>Ganesh Vilas</given-names>
</name>
<xref ref-type="aff" rid="AFF0001"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="AFF0002"><sup>b</sup>
</xref>
<xref ref-type="author-notes" rid="FT0001"><sup>*</sup>
</xref>
<xref ref-type="author-notes" rid="FT0002"><sup>†</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-9894-1938</contrib-id>
<name><surname>Yin</surname>
<given-names>Yanan</given-names>
</name>
<xref ref-type="aff" rid="AFF0001"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="AFF0003"><sup>c</sup>
</xref>
<xref ref-type="author-notes" rid="FT0001"><sup>*</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0003-3326-1007</contrib-id>
<name><surname>Jang</surname>
<given-names>Su Chul</given-names>
</name>
<xref ref-type="aff" rid="AFF0001"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0003-1279-1746</contrib-id>
<name><surname>Lässer</surname>
<given-names>Cecilia</given-names>
</name>
<xref ref-type="aff" rid="AFF0001"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wennmalm</surname>
<given-names>Stefan</given-names>
</name>
<xref ref-type="aff" rid="AFF0004"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hoffmann</surname>
<given-names>Hans Jürgen</given-names>
</name>
<xref ref-type="aff" rid="AFF0005"><sup>e</sup>
</xref>
<xref ref-type="aff" rid="AFF0006"><sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Li</given-names>
</name>
<xref ref-type="aff" rid="AFF0007"><sup>g</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gho</surname>
<given-names>Yong Song</given-names>
</name>
<xref ref-type="aff" rid="AFF0008"><sup>h</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0003-0346-6837</contrib-id>
<name><surname>Nilsson</surname>
<given-names>Jonas Andreas</given-names>
</name>
<xref ref-type="aff" rid="AFF0002"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0001-9195-9249</contrib-id>
<name><surname>Lötvall</surname>
<given-names>Jan</given-names>
</name>
<xref ref-type="corresp" rid="AN0001"></xref>
<xref ref-type="aff" rid="AFF0001"><sup>a</sup>
</xref>
</contrib>
<aff id="AFF0001"><label>a</label>
<institution>Krefting Research Centre, Institute of Medicine, the Sahlgrenska Academy, University of Gothenburg</institution>
, Gothenburg,<country>Sweden</country>
</aff>
<aff id="AFF0002"><label>b</label>
<institution>Department of Surgery, Institute of Clinical Sciences, the Sahlgrenska Academy, University of Gothenburg</institution>
, Gothenburg,<country>Sweden</country>
</aff>
<aff id="AFF0003"><label>c</label>
<institution>Department of Biochemistry and Molecular Cell Biology, Shanghai Jiao Tong University, School of Medicine</institution>
, Shanghai,<country>China</country>
</aff>
<aff id="AFF0004"><label>d</label>
<institution>Royal Institute of Technology-KTH, Department of Applied Physics, Experimental Biomolecular Physics Group, SciLife Laboratory</institution>
, Solna,<country>Sweden</country>
</aff>
<aff id="AFF0005"><label>e</label>
<institution>Department of Clinical Medicine, Aarhus University</institution>
, Aarhus,<country>Denmark</country>
</aff>
<aff id="AFF0006"><label>f</label>
<institution>Department of respiratory and Allergy, Aarhus University Hospital</institution>
, Aarhus,<country>Denmark</country>
</aff>
<aff id="AFF0007"><label>g</label>
<institution>Department of Laboratory Medicine, Shanghai First People’s Hospital, Shanghai JiaoTong University</institution>
, Shanghai,<country>China</country>
</aff>
<aff id="AFF0008"><label>h</label>
<institution>Department of Life Sciences, Pohang University of Science and Technology</institution>
, Pohang,<country>Republic of Korea</country>
</aff>
</contrib-group>
<author-notes><corresp id="AN0001">CONTACT Jan Lötvall <email xlink:href="jan.lotvall@gu.se">jan.lotvall@gu.se</email>
<institution>Krefting Research Centre, University of Gothenburg</institution>
, <addr-line>Box 424</addr-line>
, 405 30 Gothenburg, <country>Sweden</country>
</corresp>
<fn id="FT0001"><label>*</label>
<p>These two authors contributed equally to this work.</p>
</fn>
<fn id="FT0002"><label>†</label>
<p>Current affiliation: Department of Surgery, Institute of Clinical Sciences, the Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>20</day>
<month>9</month>
<year>2019</year>
</pub-date>
<volume>8</volume>
<issue>1</issue>
<elocation-id seq="64">1650458</elocation-id>
<history><date date-type="received"><day>14</day>
<month>1</month>
<year>2019</year>
</date>
<date date-type="rev-recd"><day>24</day>
<month>6</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>25</day>
<month>7</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group on behalf of The International Society for Extracellular Vesicles.</copyright-statement>
<copyright-year>2019</copyright-year>
<copyright-holder>The Author(s)</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="ZJEV_8_1650458.pdf"></self-uri>
<abstract><title>ABSTRACT</title>
<p>Extracellular vesicles such as exosomes convey biological messages between cells, either by surface-to-surface interaction or by shuttling of bioactive molecules to a recipient cell’s cytoplasm. Here we show that exosomes released by mast cells harbour both active and latent transforming growth factor β-1 (TGFβ-1) on their surfaces. The latent form of TGFβ-1 is associated with the exosomes via heparinase-II and pH-sensitive elements. These vesicles traffic to the endocytic compartment of recipient human mesenchymal stem cells (MSCs) within 60 min of exposure. Further, the exosomes-associated TGFβ-1 is retained within the endosomal compartments at the time of signalling, which results in prolonged cellular signalling compared to free-TGFβ-1. These exosomes induce a migratory phenotype in primary MSCs involving SMAD-dependent pathways. Our results show that mast cell-derived exosomes are decorated with latent TGFβ-1 and are retained in recipient MSC endosomes, influencing recipient cell migratory phenotype. We conclude that exosomes can convey signalling within endosomes by delivering bioactive surface ligands to this intracellular compartment.</p>
</abstract>
<kwd-group kwd-group-type="author"><title>KEYWORDS</title>
<kwd>Mast cells</kwd>
<kwd>extracellular vesicles</kwd>
<kwd>exosomes</kwd>
<kwd>mesenchymal stem cells</kwd>
<kwd>tumour growth factor beta-1</kwd>
<kwd>cellular localization</kwd>
<kwd>endosomal signalling</kwd>
<kwd>proteoglycan</kwd>
</kwd-group>
<funding-group><award-group><funding-source><named-content content-type="funder-name">Cancerfonden</named-content>
<named-content content-type="funder-identifier">10.13039/501100002794</named-content>
</funding-source>
<award-id>.</award-id>
</award-group>
<award-group><funding-source><named-content content-type="funder-name">European Academy of Allergy and Clinical Immunology</named-content>
<named-content content-type="funder-identifier">10.13039/501100011824</named-content>
</funding-source>
<award-id>Long term fellowship</award-id>
</award-group>
<award-group><funding-source><named-content content-type="funder-name">Hjärt-Lungfonden</named-content>
<named-content content-type="funder-identifier">10.13039/501100003793</named-content>
</funding-source>
<award-id>2015-0588</award-id>
</award-group>
<award-group><funding-source><named-content content-type="funder-name">Sahlgrenska Akademin</named-content>
<named-content content-type="funder-identifier">10.13039/501100005761</named-content>
</funding-source>
<award-id>.</award-id>
</award-group>
<award-group><funding-source><named-content content-type="funder-name">Stiftelsen Assar Gabrielssons Fond</named-content>
<named-content content-type="funder-identifier">10.13039/501100005009</named-content>
</funding-source>
<award-id>FB16-104</award-id>
</award-group>
<award-group><funding-source><named-content content-type="funder-name">Stiftelserna Wilhelm och Martina Lundgrens</named-content>
<named-content content-type="funder-identifier">10.13039/501100003745</named-content>
</funding-source>
<award-id>2017-1842</award-id>
</award-group>
<award-group><funding-source><named-content content-type="funder-name">Vetenskapsrådet</named-content>
<named-content content-type="funder-identifier">10.13039/501100004359</named-content>
</funding-source>
<award-id>.</award-id>
</award-group>
<funding-statement>This work was supported by the intramural funding from the VBG group Herman Krefting Foundation for Allergy and Asthma Research; Swedish Cancer Foundation [CAN2014/844]; Swedish Research Council [2016-02854]; and the Swedish Heart-Lung Foundation [2015-0588]. GS was supported by European Academy of Allergy and Clinical Immunology [Long term fellowship-2012]; Assar Gabrielssons Foundation [FB16-104]; Stiftelserna Wilhelm and Martina Lundgrens [2017-1842]; Sahlgrenska Academy; and Sahlgrenska University Hospital.</funding-statement>
</funding-group>
<counts><fig-count count="7"></fig-count>
<ref-count count="60"></ref-count>
<page-count count="21"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Corée du Sud</li>
<li>Danemark</li>
<li>République populaire de Chine</li>
<li>Suède</li>
</country>
</list>
<tree><country name="Suède"><noRegion><name sortKey="Shelke, Ganesh Vilas" sort="Shelke, Ganesh Vilas" uniqKey="Shelke G" first="Ganesh Vilas" last="Shelke">Ganesh Vilas Shelke</name>
</noRegion>
<name sortKey="Jang, Su Chul" sort="Jang, Su Chul" uniqKey="Jang S" first="Su Chul" last="Jang">Su Chul Jang</name>
<name sortKey="L Sser, Cecilia" sort="L Sser, Cecilia" uniqKey="L Sser C" first="Cecilia" last="L Sser">Cecilia L Sser</name>
<name sortKey="Lotvall, Jan" sort="Lotvall, Jan" uniqKey="Lotvall J" first="Jan" last="Lötvall">Jan Lötvall</name>
<name sortKey="Nilsson, Jonas Andreas" sort="Nilsson, Jonas Andreas" uniqKey="Nilsson J" first="Jonas Andreas" last="Nilsson">Jonas Andreas Nilsson</name>
<name sortKey="Shelke, Ganesh Vilas" sort="Shelke, Ganesh Vilas" uniqKey="Shelke G" first="Ganesh Vilas" last="Shelke">Ganesh Vilas Shelke</name>
<name sortKey="Wennmalm, Stefan" sort="Wennmalm, Stefan" uniqKey="Wennmalm S" first="Stefan" last="Wennmalm">Stefan Wennmalm</name>
<name sortKey="Yin, Yanan" sort="Yin, Yanan" uniqKey="Yin Y" first="Yanan" last="Yin">Yanan Yin</name>
</country>
<country name="République populaire de Chine"><noRegion><name sortKey="Yin, Yanan" sort="Yin, Yanan" uniqKey="Yin Y" first="Yanan" last="Yin">Yanan Yin</name>
</noRegion>
<name sortKey="Li, Li" sort="Li, Li" uniqKey="Li L" first="Li" last="Li">Li Li</name>
</country>
<country name="Danemark"><noRegion><name sortKey="Hoffmann, Hans Jurgen" sort="Hoffmann, Hans Jurgen" uniqKey="Hoffmann H" first="Hans Jürgen" last="Hoffmann">Hans Jürgen Hoffmann</name>
</noRegion>
<name sortKey="Hoffmann, Hans Jurgen" sort="Hoffmann, Hans Jurgen" uniqKey="Hoffmann H" first="Hans Jürgen" last="Hoffmann">Hans Jürgen Hoffmann</name>
</country>
<country name="Corée du Sud"><noRegion><name sortKey="Gho, Yong Song" sort="Gho, Yong Song" uniqKey="Gho Y" first="Yong Song" last="Gho">Yong Song Gho</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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