Tissue Factor Induced by Epithelial-Mesenchymal Transition Triggers a Procoagulant State That Drives Metastasis of Circulating Tumor Cells.
Identifieur interne : 001484 ( PubMed/Checkpoint ); précédent : 001483; suivant : 001485Tissue Factor Induced by Epithelial-Mesenchymal Transition Triggers a Procoagulant State That Drives Metastasis of Circulating Tumor Cells.
Auteurs : Morgane Bourcy [Belgique] ; Meggy Suarez-Carmona [Belgique] ; Justine Lambert [Belgique] ; Marie-Emilie Francart [Belgique] ; Hélène Schroeder [Belgique] ; Céline Delierneux [Belgique] ; Nicolas Skrypek [Belgique] ; Erik W. Thompson [Australie] ; Guy Jérusalem [Belgique] ; Geert Berx [Belgique] ; Marc Thiry [Belgique] ; Silvia Blacher [Belgique] ; Brett G. Hollier [Australie] ; Agnès Noël [Belgique] ; Cécile Oury [Belgique] ; Myriam Polette [France] ; Christine Gilles [Belgique]Source :
- Cancer research [ 1538-7445 ] ; 2016.
Descripteurs français
- KwdFr :
- Animaux, Cellules tumorales circulantes (anatomopathologie), Coagulation sanguine, Facteur de transcription Zeb1 (physiologie), Femelle, Humains, Lignée cellulaire tumorale, Souris, Souris de lignée BALB C, Thromboplastine (biosynthèse), Transition épithélio-mésenchymateuse, Tumeurs du poumon (secondaire).
- MESH :
- anatomopathologie : Cellules tumorales circulantes.
- biosynthèse : Thromboplastine.
- physiologie : Facteur de transcription Zeb1.
- secondaire : Tumeurs du poumon.
- Animaux, Coagulation sanguine, Femelle, Humains, Lignée cellulaire tumorale, Souris, Souris de lignée BALB C, Transition épithélio-mésenchymateuse.
English descriptors
- KwdEn :
- MESH :
- chemical , biosynthesis : Thromboplastin.
- pathology : Neoplastic Cells, Circulating.
- chemical , physiology : Zinc Finger E-box-Binding Homeobox 1.
- secondary : Lung Neoplasms.
- Animals, Blood Coagulation, Cell Line, Tumor, Epithelial-Mesenchymal Transition, Female, Humans, Mice, Mice, Inbred BALB C.
Abstract
Epithelial-mesenchymal transition (EMT) is prominent in circulating tumor cells (CTC), but how it influences metastatic spread in this setting is obscure. Insofar as blood provides a specific microenvironment for tumor cells, we explored a potential link between EMT and coagulation that may provide EMT-positive CTCs with enhanced colonizing properties. Here we report that EMT induces tissue factor (TF), a major cell-associated initiator of coagulation and related procoagulant properties in the blood. TF blockade by antibody or shRNA diminished the procoagulant activity of EMT-positive cells, confirming a functional role for TF in these processes. Silencing the EMT transcription factor ZEB1 inhibited both EMT-associated TF expression and coagulant activity, further strengthening the link between EMT and coagulation. Accordingly, EMT-positive cells exhibited a higher persistance/survival in the lungs of mice colonized after intravenous injection, a feature diminished by TF or ZEB1 silencing. In tumor cells with limited metastatic capability, enforcing expression of the EMT transcription factor Snail increased TF, coagulant properties, and early metastasis. Clinically, we identified a subpopulation of CTC expressing vimentin and TF in the blood of metastatic breast cancer patients consistent with our observations. Overall, our findings define a novel EMT-TF regulatory axis that triggers local activation of coagulation pathways to support metastatic colonization of EMT-positive CTCs. Cancer Res; 76(14); 4270-82. ©2016 AACR.
DOI: 10.1158/0008-5472.CAN-15-2263
PubMed: 27221703
Affiliations:
- Australie, Belgique, France
- Champagne-Ardenne, Grand Est, Province de Flandre-Orientale, Province de Liège, Région flamande, Région wallonne
- Gand, Liège, Reims
- Université de Gand, Université de Liège
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pubmed:27221703Le document en format XML
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<author><name sortKey="Gilles, Christine" sort="Gilles, Christine" uniqKey="Gilles C" first="Christine" last="Gilles">Christine Gilles</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">Tissue Factor Induced by Epithelial-Mesenchymal Transition Triggers a Procoagulant State That Drives Metastasis of Circulating Tumor Cells.</title>
<author><name sortKey="Bourcy, Morgane" sort="Bourcy, Morgane" uniqKey="Bourcy M" first="Morgane" last="Bourcy">Morgane Bourcy</name>
<affiliation wicri:level="4"><nlm:affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</nlm:affiliation>
<country xml:lang="fr">Belgique</country>
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<author><name sortKey="Suarez Carmona, Meggy" sort="Suarez Carmona, Meggy" uniqKey="Suarez Carmona M" first="Meggy" last="Suarez-Carmona">Meggy Suarez-Carmona</name>
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<author><name sortKey="Francart, Marie Emilie" sort="Francart, Marie Emilie" uniqKey="Francart M" first="Marie-Emilie" last="Francart">Marie-Emilie Francart</name>
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<author><name sortKey="Schroeder, Helene" sort="Schroeder, Helene" uniqKey="Schroeder H" first="Hélène" last="Schroeder">Hélène Schroeder</name>
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<author><name sortKey="Delierneux, Celine" sort="Delierneux, Celine" uniqKey="Delierneux C" first="Céline" last="Delierneux">Céline Delierneux</name>
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<author><name sortKey="Thompson, Erik W" sort="Thompson, Erik W" uniqKey="Thompson E" first="Erik W" last="Thompson">Erik W. Thompson</name>
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<author><name sortKey="Jerusalem, Guy" sort="Jerusalem, Guy" uniqKey="Jerusalem G" first="Guy" last="Jérusalem">Guy Jérusalem</name>
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<wicri:regionArea>CHU, Department of Medical Oncology, University of Liège, Liège</wicri:regionArea>
<orgName type="university">Université de Liège</orgName>
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<author><name sortKey="Berx, Geert" sort="Berx, Geert" uniqKey="Berx G" first="Geert" last="Berx">Geert Berx</name>
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<author><name sortKey="Polette, Myriam" sort="Polette, Myriam" uniqKey="Polette M" first="Myriam" last="Polette">Myriam Polette</name>
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<author><name sortKey="Gilles, Christine" sort="Gilles, Christine" uniqKey="Gilles C" first="Christine" last="Gilles">Christine Gilles</name>
<affiliation wicri:level="4"><nlm:affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium. cgilles@ulg.ac.be.</nlm:affiliation>
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<series><title level="j">Cancer research</title>
<idno type="eISSN">1538-7445</idno>
<imprint><date when="2016" type="published">2016</date>
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<term>Blood Coagulation</term>
<term>Cell Line, Tumor</term>
<term>Epithelial-Mesenchymal Transition</term>
<term>Female</term>
<term>Humans</term>
<term>Lung Neoplasms (secondary)</term>
<term>Mice</term>
<term>Mice, Inbred BALB C</term>
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<term>Thromboplastin (biosynthesis)</term>
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<term>Humains</term>
<term>Lignée cellulaire tumorale</term>
<term>Souris</term>
<term>Souris de lignée BALB C</term>
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<term>Transition épithélio-mésenchymateuse</term>
<term>Tumeurs du poumon (secondaire)</term>
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<front><div type="abstract" xml:lang="en">Epithelial-mesenchymal transition (EMT) is prominent in circulating tumor cells (CTC), but how it influences metastatic spread in this setting is obscure. Insofar as blood provides a specific microenvironment for tumor cells, we explored a potential link between EMT and coagulation that may provide EMT-positive CTCs with enhanced colonizing properties. Here we report that EMT induces tissue factor (TF), a major cell-associated initiator of coagulation and related procoagulant properties in the blood. TF blockade by antibody or shRNA diminished the procoagulant activity of EMT-positive cells, confirming a functional role for TF in these processes. Silencing the EMT transcription factor ZEB1 inhibited both EMT-associated TF expression and coagulant activity, further strengthening the link between EMT and coagulation. Accordingly, EMT-positive cells exhibited a higher persistance/survival in the lungs of mice colonized after intravenous injection, a feature diminished by TF or ZEB1 silencing. In tumor cells with limited metastatic capability, enforcing expression of the EMT transcription factor Snail increased TF, coagulant properties, and early metastasis. Clinically, we identified a subpopulation of CTC expressing vimentin and TF in the blood of metastatic breast cancer patients consistent with our observations. Overall, our findings define a novel EMT-TF regulatory axis that triggers local activation of coagulation pathways to support metastatic colonization of EMT-positive CTCs. Cancer Res; 76(14); 4270-82. ©2016 AACR.</div>
</front>
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<DateCreated><Year>2016</Year>
<Month>09</Month>
<Day>22</Day>
</DateCreated>
<DateCompleted><Year>2017</Year>
<Month>07</Month>
<Day>17</Day>
</DateCompleted>
<DateRevised><Year>2017</Year>
<Month>10</Month>
<Day>30</Day>
</DateRevised>
<Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1538-7445</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>76</Volume>
<Issue>14</Issue>
<PubDate><Year>2016</Year>
<Month>07</Month>
<Day>15</Day>
</PubDate>
</JournalIssue>
<Title>Cancer research</Title>
<ISOAbbreviation>Cancer Res.</ISOAbbreviation>
</Journal>
<ArticleTitle>Tissue Factor Induced by Epithelial-Mesenchymal Transition Triggers a Procoagulant State That Drives Metastasis of Circulating Tumor Cells.</ArticleTitle>
<Pagination><MedlinePgn>4270-82</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1158/0008-5472.CAN-15-2263</ELocationID>
<Abstract><AbstractText>Epithelial-mesenchymal transition (EMT) is prominent in circulating tumor cells (CTC), but how it influences metastatic spread in this setting is obscure. Insofar as blood provides a specific microenvironment for tumor cells, we explored a potential link between EMT and coagulation that may provide EMT-positive CTCs with enhanced colonizing properties. Here we report that EMT induces tissue factor (TF), a major cell-associated initiator of coagulation and related procoagulant properties in the blood. TF blockade by antibody or shRNA diminished the procoagulant activity of EMT-positive cells, confirming a functional role for TF in these processes. Silencing the EMT transcription factor ZEB1 inhibited both EMT-associated TF expression and coagulant activity, further strengthening the link between EMT and coagulation. Accordingly, EMT-positive cells exhibited a higher persistance/survival in the lungs of mice colonized after intravenous injection, a feature diminished by TF or ZEB1 silencing. In tumor cells with limited metastatic capability, enforcing expression of the EMT transcription factor Snail increased TF, coagulant properties, and early metastasis. Clinically, we identified a subpopulation of CTC expressing vimentin and TF in the blood of metastatic breast cancer patients consistent with our observations. Overall, our findings define a novel EMT-TF regulatory axis that triggers local activation of coagulation pathways to support metastatic colonization of EMT-positive CTCs. Cancer Res; 76(14); 4270-82. ©2016 AACR.</AbstractText>
<CopyrightInformation>©2016 American Association for Cancer Research.</CopyrightInformation>
</Abstract>
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<ForeName>Morgane</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Suarez-Carmona</LastName>
<ForeName>Meggy</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</Affiliation>
</AffiliationInfo>
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<ForeName>Justine</ForeName>
<Initials>J</Initials>
<AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</Affiliation>
</AffiliationInfo>
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<ForeName>Marie-Emilie</ForeName>
<Initials>ME</Initials>
<AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</Affiliation>
</AffiliationInfo>
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<ForeName>Hélène</ForeName>
<Initials>H</Initials>
<AffiliationInfo><Affiliation>CHU, Department of Medical Oncology, University of Liège, Liège, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
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<ForeName>Céline</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>GIGA-Cardiovascular Sciences, Laboratory of Thrombosis and Hemostasis, University of Liège, Liège, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Skrypek</LastName>
<ForeName>Nicolas</ForeName>
<Initials>N</Initials>
<AffiliationInfo><Affiliation>Unit of Molecular and Cellular Oncology Lab, Inflammation Research Center, VIB, Ghent, Belgium. Department of Biomedical Molecular Biology, Cancer Research Institute Ghent (CRIG), Ghent University, Ghent, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Thompson</LastName>
<ForeName>Erik W</ForeName>
<Initials>EW</Initials>
<AffiliationInfo><Affiliation>Institute of Health and Biomedical Innovation and School of Biomedical Sciences Translational Research Institute, Queensland University of Technology, Brisbane, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Jérusalem</LastName>
<ForeName>Guy</ForeName>
<Initials>G</Initials>
<AffiliationInfo><Affiliation>CHU, Department of Medical Oncology, University of Liège, Liège, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Berx</LastName>
<ForeName>Geert</ForeName>
<Initials>G</Initials>
<AffiliationInfo><Affiliation>Unit of Molecular and Cellular Oncology Lab, Inflammation Research Center, VIB, Ghent, Belgium. Department of Biomedical Molecular Biology, Cancer Research Institute Ghent (CRIG), Ghent University, Ghent, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Thiry</LastName>
<ForeName>Marc</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>GIGA-Neurosciences, Unit of Cell and Tissue Biology, University of Liège, Liège, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Blacher</LastName>
<ForeName>Silvia</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Hollier</LastName>
<ForeName>Brett G</ForeName>
<Initials>BG</Initials>
<AffiliationInfo><Affiliation>Australian Prostate Cancer Research Centre - Queensland, Institute of Health and Biomedical Innovation, School of Biomedical Sciences, Queensland University of Technology, Princess Alexandra Hospital, Translational Research Institute, Brisbane, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Noël</LastName>
<ForeName>Agnès</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Oury</LastName>
<ForeName>Cécile</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>GIGA-Cardiovascular Sciences, Laboratory of Thrombosis and Hemostasis, University of Liège, Liège, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Polette</LastName>
<ForeName>Myriam</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>INSERM UMR-S 903, CHU, Biopathology Laboratory, University of Reims, Reims, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Gilles</LastName>
<ForeName>Christine</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium. cgilles@ulg.ac.be.</Affiliation>
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<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
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<Month>05</Month>
<Day>24</Day>
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<MedlineTA>Cancer Res</MedlineTA>
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<ISSNLinking>0008-5472</ISSNLinking>
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<Month>08</Month>
<Day>17</Day>
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<PubMedPubDate PubStatus="accepted"><Year>2016</Year>
<Month>04</Month>
<Day>26</Day>
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<li>France</li>
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<li>Grand Est</li>
<li>Province de Flandre-Orientale</li>
<li>Province de Liège</li>
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<li>Région wallonne</li>
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<settlement><li>Gand</li>
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<name sortKey="Blacher, Silvia" sort="Blacher, Silvia" uniqKey="Blacher S" first="Silvia" last="Blacher">Silvia Blacher</name>
<name sortKey="Delierneux, Celine" sort="Delierneux, Celine" uniqKey="Delierneux C" first="Céline" last="Delierneux">Céline Delierneux</name>
<name sortKey="Francart, Marie Emilie" sort="Francart, Marie Emilie" uniqKey="Francart M" first="Marie-Emilie" last="Francart">Marie-Emilie Francart</name>
<name sortKey="Gilles, Christine" sort="Gilles, Christine" uniqKey="Gilles C" first="Christine" last="Gilles">Christine Gilles</name>
<name sortKey="Jerusalem, Guy" sort="Jerusalem, Guy" uniqKey="Jerusalem G" first="Guy" last="Jérusalem">Guy Jérusalem</name>
<name sortKey="Lambert, Justine" sort="Lambert, Justine" uniqKey="Lambert J" first="Justine" last="Lambert">Justine Lambert</name>
<name sortKey="Noel, Agnes" sort="Noel, Agnes" uniqKey="Noel A" first="Agnès" last="Noël">Agnès Noël</name>
<name sortKey="Oury, Cecile" sort="Oury, Cecile" uniqKey="Oury C" first="Cécile" last="Oury">Cécile Oury</name>
<name sortKey="Schroeder, Helene" sort="Schroeder, Helene" uniqKey="Schroeder H" first="Hélène" last="Schroeder">Hélène Schroeder</name>
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<country name="France"><region name="Grand Est"><name sortKey="Polette, Myriam" sort="Polette, Myriam" uniqKey="Polette M" first="Myriam" last="Polette">Myriam Polette</name>
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