Tumor hypoxia modulates podoplanin/CCL21 interactions in CCR7+ NK cell recruitment and CCR7+ tumor cell mobilization
Identifieur interne : 000006 ( France/Analysis ); précédent : 000005; suivant : 000007Tumor hypoxia modulates podoplanin/CCL21 interactions in CCR7+ NK cell recruitment and CCR7+ tumor cell mobilization
Auteurs : Anna Tejchman [France, Pologne] ; Nathalie Lamerant-Fayel [France] ; Jean-Claude Jacquinet [France] ; Aleksandra Bielawska-Pohl [Pologne] ; Katarzyna Mleczko-Sanecka [France] ; Catherine Grillon [France] ; Salem Chouaib [France] ; Maciej Ugorski [Pologne] ; Claudine Kieda [France, Pologne]Source :
- Oncotarget [ 1949-2553 ] ; 2017.
Abstract
Podoplanin (PDPN), an O-glycosylated, transmembrane, mucin-type glycoprotein, is expressed by cancer associated fibroblasts (CAFs). In malignant transformation, PDPN is subjected to changes and its role is yet to be established. Here we show that it is involved in modulating the activity of the CCL21/CCR7 chemokine/receptor axis in a hypoxia-dependent manner. In the present model, breast cancer MDA-MB-231 cells and NKL3 cells express the surface CCR7 receptor for CCL21 chemokine which is a potent chemoattractant able to bind to PDPN. The impact of the CCL21/CCR7 axis in the molecular mechanism of the adhesion of NKL3 cells and of MDA-MB-231 breast cancer cells was reduced in a hypoxic tumor environment. In addition to its known effect on migration, CCL21/CCR7 interaction was shown to allow NK cell adhesion to endothelial cells (ECs) and its reduction by hypoxia. A PDPN expressing model of CAFs made it possible to demonstrate the same CCL21/CCR7 axis involvement in the tumor cells to CAFs recognition mechanism through PDPN binding of CCL21. PDPN was induced by hypoxia and its overexpression undergoes a reduction of adhesion, making it an anti-adhesion molecule in the absence of CCL21, in the tumor. CCL21/CCR7 modulated NK cells/ECs and MDA-MB-231 cells/CAF PDPN-dependent interactions were further shown to be linked to hypoxia-dependent microRNAs as miRs: miR-210 and specifically miR-21, miR-29b which influence PDPN expression.
Url:
DOI: 10.18632/oncotarget.16311
PubMed: 28416768
PubMed Central: 5458255
Affiliations:
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PMC:5458255Le document en format XML
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Centre</region><settlement type="city">Orléans</settlement></placeName></affiliation></author><author><name sortKey="Jacquinet, Jean Claude" sort="Jacquinet, Jean Claude" uniqKey="Jacquinet J" first="Jean-Claude" last="Jacquinet">Jean-Claude Jacquinet</name><affiliation wicri:level="3"><nlm:aff id="A3"> ICOA, UMR CNRS 7311, University of Orleans, Orleans, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea> ICOA, UMR CNRS 7311, University of Orleans, Orleans</wicri:regionArea><placeName><region type="region">Centre-Val de Loire</region><region type="old region">Région Centre</region><settlement type="city">Orléans</settlement></placeName></affiliation></author><author><name sortKey="Bielawska Pohl, Aleksandra" sort="Bielawska Pohl, Aleksandra" uniqKey="Bielawska Pohl A" first="Aleksandra" last="Bielawska-Pohl">Aleksandra Bielawska-Pohl</name><affiliation wicri:level="1"><nlm:aff id="A2"> Laboratory of Glycobiology and Intercellular Interactions, Institute of Immunology and Experimental Therapy, PAN, Wroclaw, Poland</nlm:aff><country xml:lang="fr">Pologne</country><wicri:regionArea> Laboratory of Glycobiology and Intercellular Interactions, Institute of Immunology and Experimental Therapy, PAN, Wroclaw</wicri:regionArea><wicri:noRegion>Wroclaw</wicri:noRegion></affiliation></author><author><name sortKey="Mleczko Sanecka, Katarzyna" sort="Mleczko Sanecka, Katarzyna" uniqKey="Mleczko Sanecka K" first="Katarzyna" last="Mleczko-Sanecka">Katarzyna Mleczko-Sanecka</name><affiliation wicri:level="3"><nlm:aff id="A1"> Centre for Molecular Biophysics, UPR 4301 CNRS affiliated to Orléans University and INSERM, Orléans, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea> Centre for Molecular Biophysics, UPR 4301 CNRS affiliated to Orléans University and INSERM, Orléans</wicri:regionArea><placeName><region type="region">Centre-Val de Loire</region><region type="old region">Région Centre</region><settlement type="city">Orléans</settlement></placeName></affiliation></author><author><name sortKey="Grillon, Catherine" sort="Grillon, Catherine" uniqKey="Grillon C" first="Catherine" last="Grillon">Catherine Grillon</name><affiliation wicri:level="3"><nlm:aff id="A1"> Centre for Molecular Biophysics, UPR 4301 CNRS affiliated to Orléans University and INSERM, Orléans, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea> Centre for Molecular Biophysics, UPR 4301 CNRS affiliated to Orléans University and INSERM, Orléans</wicri:regionArea><placeName><region type="region">Centre-Val de Loire</region><region type="old region">Région Centre</region><settlement type="city">Orléans</settlement></placeName></affiliation></author><author><name sortKey="Chouaib, Salem" sort="Chouaib, Salem" uniqKey="Chouaib S" first="Salem" last="Chouaib">Salem Chouaib</name><affiliation wicri:level="1"><nlm:aff id="A4"> INSERM U1186, Gustave Roussy Institute, Villejuif, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea> INSERM U1186, Gustave Roussy Institute, Villejuif</wicri:regionArea><wicri:noRegion>Villejuif</wicri:noRegion><wicri:noRegion>Villejuif</wicri:noRegion></affiliation></author><author><name sortKey="Ugorski, Maciej" sort="Ugorski, Maciej" uniqKey="Ugorski M" first="Maciej" last="Ugorski">Maciej Ugorski</name><affiliation wicri:level="1"><nlm:aff id="A2"> Laboratory of Glycobiology and Intercellular Interactions, Institute of Immunology and Experimental Therapy, PAN, Wroclaw, Poland</nlm:aff><country xml:lang="fr">Pologne</country><wicri:regionArea> Laboratory of Glycobiology and Intercellular Interactions, Institute of Immunology and Experimental Therapy, PAN, Wroclaw</wicri:regionArea><wicri:noRegion>Wroclaw</wicri:noRegion></affiliation></author><author><name sortKey="Kieda, Claudine" sort="Kieda, Claudine" uniqKey="Kieda C" first="Claudine" last="Kieda">Claudine Kieda</name><affiliation wicri:level="3"><nlm:aff id="A1"> Centre for Molecular Biophysics, UPR 4301 CNRS affiliated to Orléans University and INSERM, Orléans, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea> Centre for Molecular Biophysics, UPR 4301 CNRS affiliated to Orléans University and INSERM, Orléans</wicri:regionArea><placeName><region type="region">Centre-Val de Loire</region><region type="old region">Région Centre</region><settlement type="city">Orléans</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:aff id="A5"> Malopolska Centre of Biotechnology, Jagiellonian University, Krakow, Poland</nlm:aff><country xml:lang="fr">Pologne</country><wicri:regionArea> Malopolska Centre of Biotechnology, Jagiellonian University, Krakow</wicri:regionArea><wicri:noRegion>Krakow</wicri:noRegion></affiliation></author></analytic><series><title level="j">Oncotarget</title><idno type="eISSN">1949-2553</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Podoplanin (PDPN), an O-glycosylated, transmembrane, mucin-type glycoprotein, is expressed by cancer associated fibroblasts (CAFs). In malignant transformation, PDPN is subjected to changes and its role is yet to be established. Here we show that it is involved in modulating the activity of the CCL21/CCR7 chemokine/receptor axis in a hypoxia-dependent manner. In the present model, breast cancer MDA-MB-231 cells and NKL3 cells express the surface CCR7 receptor for CCL21 chemokine which is a potent chemoattractant able to bind to PDPN. The impact of the CCL21/CCR7 axis in the molecular mechanism of the adhesion of NKL3 cells and of MDA-MB-231 breast cancer cells was reduced in a hypoxic tumor environment. In addition to its known effect on migration, CCL21/CCR7 interaction was shown to allow NK cell adhesion to endothelial cells (ECs) and its reduction by hypoxia. A PDPN expressing model of CAFs made it possible to demonstrate the same CCL21/CCR7 axis involvement in the tumor cells to CAFs recognition mechanism through PDPN binding of CCL21. PDPN was induced by hypoxia and its overexpression undergoes a reduction of adhesion, making it an anti-adhesion molecule in the absence of CCL21, in the tumor. CCL21/CCR7 modulated NK cells/ECs and MDA-MB-231 cells/CAF PDPN-dependent interactions were further shown to be linked to hypoxia-dependent microRNAs as miRs: miR-210 and specifically miR-21, miR-29b which influence PDPN expression.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Gunn, Md" uniqKey="Gunn M">MD Gunn</name></author><author><name sortKey="Tangemann, K" uniqKey="Tangemann K">K Tangemann</name></author><author><name sortKey="Tam, C" uniqKey="Tam C">C Tam</name></author><author><name sortKey="Cyster, Jg" uniqKey="Cyster J">JG Cyster</name></author><author><name sortKey="Rosen, Sd" uniqKey="Rosen S">SD Rosen</name></author><author><name sortKey="Williams, Lt" uniqKey="Williams L">LT Williams</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yoshida, R" uniqKey="Yoshida R">R Yoshida</name></author><author><name sortKey="Imai, T" uniqKey="Imai T">T Imai</name></author><author><name 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M">MS Brassesco</name></author><author><name sortKey="Scrideli, Ca" uniqKey="Scrideli C">CA Scrideli</name></author><author><name sortKey="Tone, Lg" uniqKey="Tone L">LG Tone</name></author><author><name sortKey="Georgescu, M" uniqKey="Georgescu M">M Georgescu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Cie Lar Pobuda, A" uniqKey="Cie Lar Pobuda A">A Cieślar-Pobuda</name></author><author><name sortKey="Jain, Mv" uniqKey="Jain M">MV Jain</name></author><author><name sortKey="Kratz, G" uniqKey="Kratz G">G Kratz</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Akbari Birgani, S" uniqKey="Akbari Birgani S">S Akbari-birgani</name></author><author><name sortKey="Paranjothy, T" uniqKey="Paranjothy T">T Paranjothy</name></author><author><name sortKey="Zuse, A" uniqKey="Zuse A">A Zuse</name></author><author><name sortKey="Janikowski, T" uniqKey="Janikowski T">T Janikowski</name></author><author><name sortKey="Likus, W" uniqKey="Likus W">W Likus</name></author><author><name sortKey="Cies, A" uniqKey="Cies A">A Cies</name></author><author><name sortKey="Schweizer, F" uniqKey="Schweizer F">F Schweizer</name></author><author><name sortKey="Ghavami, S" uniqKey="Ghavami S">S Ghavami</name></author><author><name sortKey="Klonisch, T" uniqKey="Klonisch T">T Klonisch</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Guezguez, B" uniqKey="Guezguez B">B Guezguez</name></author><author><name sortKey="Vigneron, P" uniqKey="Vigneron P">P Vigneron</name></author><author><name sortKey="Lamerant, N" uniqKey="Lamerant N">N Lamerant</name></author><author><name sortKey="Kieda, C" uniqKey="Kieda C">C Kieda</name></author><author><name sortKey="Jaffredo, T" uniqKey="Jaffredo T">T Jaffredo</name></author><author><name sortKey="Dunon, D" uniqKey="Dunon D">D Dunon</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mokdaire, Cdb" uniqKey="Mokdaire C">CDB Mokdaire</name></author><author><name sortKey="Haute, R" uniqKey="Haute R">R Haute</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>France</li><li>Pologne</li></country><region><li>Centre-Val de Loire</li><li>Région Centre</li></region><settlement><li>Orléans</li></settlement></list><tree><country name="France"><region name="Centre-Val de Loire"><name sortKey="Tejchman, Anna" sort="Tejchman, Anna" uniqKey="Tejchman A" first="Anna" last="Tejchman">Anna Tejchman</name></region><name sortKey="Chouaib, Salem" sort="Chouaib, Salem" uniqKey="Chouaib S" first="Salem" last="Chouaib">Salem Chouaib</name><name sortKey="Grillon, Catherine" sort="Grillon, Catherine" uniqKey="Grillon C" first="Catherine" last="Grillon">Catherine Grillon</name><name sortKey="Jacquinet, Jean Claude" sort="Jacquinet, Jean Claude" uniqKey="Jacquinet J" first="Jean-Claude" last="Jacquinet">Jean-Claude Jacquinet</name><name sortKey="Kieda, Claudine" sort="Kieda, Claudine" uniqKey="Kieda C" first="Claudine" last="Kieda">Claudine Kieda</name><name sortKey="Lamerant Fayel, Nathalie" sort="Lamerant Fayel, Nathalie" uniqKey="Lamerant Fayel N" first="Nathalie" last="Lamerant-Fayel">Nathalie Lamerant-Fayel</name><name sortKey="Mleczko Sanecka, Katarzyna" sort="Mleczko Sanecka, Katarzyna" uniqKey="Mleczko Sanecka K" first="Katarzyna" last="Mleczko-Sanecka">Katarzyna Mleczko-Sanecka</name></country><country name="Pologne"><noRegion><name sortKey="Tejchman, Anna" sort="Tejchman, Anna" uniqKey="Tejchman A" first="Anna" last="Tejchman">Anna Tejchman</name></noRegion><name sortKey="Bielawska Pohl, Aleksandra" sort="Bielawska Pohl, Aleksandra" uniqKey="Bielawska Pohl A" first="Aleksandra" last="Bielawska-Pohl">Aleksandra Bielawska-Pohl</name><name sortKey="Kieda, Claudine" sort="Kieda, Claudine" uniqKey="Kieda C" first="Claudine" last="Kieda">Claudine Kieda</name><name sortKey="Ugorski, Maciej" sort="Ugorski, Maciej" uniqKey="Ugorski M" first="Maciej" last="Ugorski">Maciej Ugorski</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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