VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing Notch signalling
Identifieur interne : 000293 ( France/Analysis ); précédent : 000292; suivant : 000294VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing Notch signalling
Auteurs : Tuomas Tammela [Finlande] ; Georgia Zarkada [Finlande] ; Harri Nurmi [Finlande] ; Lars Jakobsson [Royaume-Uni] ; Krista Heinolainen [Finlande] ; Denis Tvorogov [Finlande] ; Wei Zheng [Finlande] ; Claudio A. Franco [Royaume-Uni] ; Aino Murtomki [Finlande] ; Evelyn Aranda [États-Unis] ; Naoyuki Miura [Japon] ; Seppo Yl-Herttuala [Finlande] ; Marcus Fruttiger [Royaume-Uni] ; Taija Mkinen [Finlande] ; Anne Eichmann [France] ; Jeffrey W. Pollard [États-Unis] ; Holger Gerhardt [Royaume-Uni, Belgique] ; Kari Alitalo [Finlande]Source :
- Nature Cell Biology [ 1465-7392 ] ; 2011-10.
Abstract
Angiogenesis, the growth of new blood vessels, involves specification of endothelial cells to tip cells and stalk cells, which is controlled by Notch signalling, whereas vascular endothelial growth factor receptor (VEGFR)-2 and VEGFR-3 have been implicated in angiogenic sprouting. Surprisingly, we found that endothelial deletion ofVegfr3, but not VEGFR-3-blocking antibodies, postnatally led to excessive angiogenic sprouting and branching, and decreased the level of Notch signalling, indicating that VEGFR-3 possesses passive and active signalling modalities. Furthermore, macrophages expressing the VEGFR-3 and VEGFR-2 ligand VEGF-C localized to vessel branch points, and Vegfc heterozygous mice exhibited inefficient angiogenesis characterized by decreased vascular branching. FoxC2 is a known regulator of Notch ligand and target gene expression, andFoxc2+/;Vegfr3+/ compound heterozygosity recapitulated homozygous loss of Vegfr3. These results indicate that macrophage-derived VEGF-C activates VEGFR-3 in tip cells to reinforce Notch signalling, which contributes to the phenotypic conversion of endothelial cells at fusion points of vessel sprouts.
Url:
- https://api.istex.fr/document/49F406354800E8A57C0A259A68D77313DF34BDAA/fulltext/pdf
- http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3261765
DOI: 10.1038/ncb2331
Affiliations:
- Belgique, Finlande, France, Japon, Royaume-Uni, États-Unis
- Angleterre, Grand Londres, Uusimaa, Île-de-France
- Helsinki, Londres, Paris
- University College de Londres, Université d'Helsinki
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ISTEX:49F406354800E8A57C0A259A68D77313DF34BDAALe document en format XML
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3PX</wicri:noRegion></affiliation></author><author><name sortKey="Heinolainen, Krista" sort="Heinolainen, Krista" uniqKey="Heinolainen K" first="Krista" last="Heinolainen">Krista Heinolainen</name><affiliation wicri:level="4"><country xml:lang="fr">Finlande</country><wicri:regionArea>Molecular/Cancer Biology Laboratory, Institute for Molecular Medicine Finland, Research Programs Unit and Department of Pathology, Haartman Institute, Biomedicum Helsinki, PO Box 63 (Haartmaninkatu 8), 00014 University of Helsinki</wicri:regionArea><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName><orgName type="university">Université d'Helsinki</orgName></affiliation></author><author><name sortKey="Tvorogov, Denis" sort="Tvorogov, Denis" uniqKey="Tvorogov D" first="Denis" last="Tvorogov">Denis Tvorogov</name><affiliation wicri:level="4"><country xml:lang="fr">Finlande</country><wicri:regionArea>Molecular/Cancer Biology Laboratory, Institute for Molecular Medicine Finland, Research Programs Unit and Department of Pathology, Haartman Institute, Biomedicum Helsinki, PO Box 63 (Haartmaninkatu 8), 00014 University of Helsinki</wicri:regionArea><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName><orgName type="university">Université d'Helsinki</orgName></affiliation></author><author><name sortKey="Zheng, Wei" sort="Zheng, Wei" uniqKey="Zheng W" first="Wei" last="Zheng">Wei Zheng</name><affiliation wicri:level="4"><country xml:lang="fr">Finlande</country><wicri:regionArea>Molecular/Cancer Biology Laboratory, Institute for Molecular Medicine Finland, Research Programs Unit and Department of Pathology, Haartman Institute, Biomedicum Helsinki, PO Box 63 (Haartmaninkatu 8), 00014 University of Helsinki</wicri:regionArea><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName><orgName type="university">Université d'Helsinki</orgName></affiliation></author><author><name sortKey="Franco, Claudio A" sort="Franco, Claudio A" uniqKey="Franco C" first="Claudio A." last="Franco">Claudio A. Franco</name><affiliation wicri:level="1"><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Vascular Biology Laboratory, London Research InstituteCancer Research UK, 44 Lincolns Inn Fields, London WC2A 3PX</wicri:regionArea><wicri:noRegion>London WC2A 3PX</wicri:noRegion></affiliation></author><author><name sortKey="Murtomki, Aino" sort="Murtomki, Aino" uniqKey="Murtomki A" first="Aino" last="Murtomki">Aino Murtomki</name><affiliation wicri:level="4"><country xml:lang="fr">Finlande</country><wicri:regionArea>Molecular/Cancer Biology Laboratory, Institute for Molecular Medicine Finland, Research Programs Unit and Department of Pathology, Haartman Institute, Biomedicum Helsinki, PO Box 63 (Haartmaninkatu 8), 00014 University of Helsinki</wicri:regionArea><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName><orgName type="university">Université d'Helsinki</orgName></affiliation></author><author><name sortKey="Aranda, Evelyn" sort="Aranda, Evelyn" uniqKey="Aranda E" first="Evelyn" last="Aranda">Evelyn Aranda</name><affiliation wicri:level="1"><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Developmental and Molecular Biology, Albert Einstein College of Medicine, New York, New York 10461</wicri:regionArea><wicri:noRegion>New York 10461</wicri:noRegion></affiliation></author><author><name sortKey="Miura, Naoyuki" sort="Miura, Naoyuki" uniqKey="Miura N" first="Naoyuki" last="Miura">Naoyuki Miura</name><affiliation wicri:level="1"><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biochemistry, Hamamatsu University School of Medicine,431-3192 Hamamatsu</wicri:regionArea><wicri:noRegion>431-3192 Hamamatsu</wicri:noRegion></affiliation></author><author><name sortKey="Yl Herttuala, Seppo" sort="Yl Herttuala, Seppo" uniqKey="Yl Herttuala S" first="Seppo" last="Yl-Herttuala">Seppo Yl-Herttuala</name><affiliation wicri:level="1"><country xml:lang="fr">Finlande</country><wicri:regionArea>A. I. Virtanen Institute and Department of Medicine, University of Kuopio, PO Box 1627, 70211 Kuopio</wicri:regionArea><wicri:noRegion>70211 Kuopio</wicri:noRegion></affiliation></author><author><name sortKey="Fruttiger, Marcus" sort="Fruttiger, Marcus" uniqKey="Fruttiger M" first="Marcus" last="Fruttiger">Marcus Fruttiger</name><affiliation wicri:level="4"><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Institute of Ophthalmology, University College London, London EC1V 9EL</wicri:regionArea><orgName type="university">University College de Londres</orgName><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Mkinen, Taija" sort="Mkinen, Taija" uniqKey="Mkinen T" first="Taija" last="Mkinen">Taija Mkinen</name><affiliation wicri:level="4"><country xml:lang="fr">Finlande</country><wicri:regionArea>Molecular/Cancer Biology Laboratory, Institute for Molecular Medicine Finland, Research Programs Unit and Department of Pathology, Haartman Institute, Biomedicum Helsinki, PO Box 63 (Haartmaninkatu 8), 00014 University of Helsinki</wicri:regionArea><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName><orgName type="university">Université d'Helsinki</orgName></affiliation></author><author><name sortKey="Eichmann, Anne" sort="Eichmann, Anne" uniqKey="Eichmann A" first="Anne" last="Eichmann">Anne Eichmann</name><affiliation wicri:level="1"><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Sant et de la Recherche Mdicale U833, Collge de France, 11 Place Marcelin Berthelot, 75005 Paris</wicri:regionArea><placeName><settlement type="city">Paris</settlement><region type="région" nuts="2">Île-de-France</region></placeName></affiliation></author><author><name sortKey="Pollard, Jeffrey W" sort="Pollard, Jeffrey W" uniqKey="Pollard J" first="Jeffrey W." last="Pollard">Jeffrey W. Pollard</name><affiliation wicri:level="1"><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Developmental and Molecular Biology, Albert Einstein College of Medicine, New York, New York 10461</wicri:regionArea><wicri:noRegion>New York 10461</wicri:noRegion></affiliation></author><author><name sortKey="Gerhardt, Holger" sort="Gerhardt, Holger" uniqKey="Gerhardt H" first="Holger" last="Gerhardt">Holger Gerhardt</name><affiliation wicri:level="1"><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Vascular Biology Laboratory, London Research InstituteCancer Research UK, 44 Lincolns Inn Fields, London WC2A 3PX</wicri:regionArea><wicri:noRegion>London WC2A 3PX</wicri:noRegion></affiliation><affiliation wicri:level="1"><country xml:lang="fr">Belgique</country><wicri:regionArea>Vascular Patterning Laboratory, Vesalius Research Center, VIB, Campus Gasthuisberg, B-3000 Leuven</wicri:regionArea><wicri:noRegion>B-3000 Leuven</wicri:noRegion></affiliation></author><author><name sortKey="Alitalo, Kari" sort="Alitalo, Kari" uniqKey="Alitalo K" first="Kari" last="Alitalo">Kari Alitalo</name><affiliation wicri:level="4"><country xml:lang="fr">Finlande</country><wicri:regionArea>Molecular/Cancer Biology Laboratory, Institute for Molecular Medicine Finland, Research Programs Unit and Department of Pathology, Haartman Institute, Biomedicum Helsinki, PO Box 63 (Haartmaninkatu 8), 00014 University of Helsinki</wicri:regionArea><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName><orgName type="university">Université d'Helsinki</orgName><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName><orgName type="university">Université d'Helsinki</orgName></affiliation><affiliation wicri:level="1"><country wicri:rule="url">Finlande</country><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName><orgName type="university">Université d'Helsinki</orgName></affiliation></author></analytic><monogr></monogr><series><title level="j">Nature Cell Biology</title><idno type="ISSN">1465-7392</idno><idno type="eISSN">1476-4679</idno><imprint><publisher>Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.</publisher><date type="published" when="2011-10">2011-10</date><biblScope unit="volume">13</biblScope><biblScope unit="issue">10</biblScope><biblScope unit="page" from="1202">1202</biblScope><biblScope unit="page" to="1213">1213</biblScope></imprint><idno type="ISSN">1465-7392</idno></series></biblStruct></sourceDesc><seriesStmt><idno type="ISSN">1465-7392</idno></seriesStmt></fileDesc><profileDesc><textClass></textClass><langUsage><language ident="en">en</language></langUsage></profileDesc></teiHeader><front><div type="abstract" xml:lang="eng">Angiogenesis, the growth of new blood vessels, involves specification of endothelial cells to tip cells and stalk cells, which is controlled by Notch signalling, whereas vascular endothelial growth factor receptor (VEGFR)-2 and VEGFR-3 have been implicated in angiogenic sprouting. Surprisingly, we found that endothelial deletion ofVegfr3, but not VEGFR-3-blocking antibodies, postnatally led to excessive angiogenic sprouting and branching, and decreased the level of Notch signalling, indicating that VEGFR-3 possesses passive and active signalling modalities. Furthermore, macrophages expressing the VEGFR-3 and VEGFR-2 ligand VEGF-C localized to vessel branch points, and Vegfc heterozygous mice exhibited inefficient angiogenesis characterized by decreased vascular branching. FoxC2 is a known regulator of Notch ligand and target gene expression, andFoxc2+/;Vegfr3+/ compound heterozygosity recapitulated homozygous loss of Vegfr3. These results indicate that macrophage-derived VEGF-C activates VEGFR-3 in tip cells to reinforce Notch signalling, which contributes to the phenotypic conversion of endothelial cells at fusion points of vessel sprouts.</div></front></TEI><affiliations><list><country><li>Belgique</li><li>Finlande</li><li>France</li><li>Japon</li><li>Royaume-Uni</li><li>États-Unis</li></country><region><li>Angleterre</li><li>Grand Londres</li><li>Uusimaa</li><li>Île-de-France</li></region><settlement><li>Helsinki</li><li>Londres</li><li>Paris</li></settlement><orgName><li>University College de Londres</li><li>Université d'Helsinki</li></orgName></list><tree><country name="Finlande"><region name="Uusimaa"><name sortKey="Tammela, Tuomas" sort="Tammela, Tuomas" uniqKey="Tammela T" first="Tuomas" last="Tammela">Tuomas Tammela</name></region><name sortKey="Alitalo, Kari" sort="Alitalo, Kari" uniqKey="Alitalo K" first="Kari" last="Alitalo">Kari Alitalo</name><name sortKey="Alitalo, Kari" sort="Alitalo, Kari" uniqKey="Alitalo K" first="Kari" last="Alitalo">Kari Alitalo</name><name sortKey="Heinolainen, Krista" sort="Heinolainen, Krista" uniqKey="Heinolainen K" first="Krista" last="Heinolainen">Krista Heinolainen</name><name sortKey="Mkinen, Taija" sort="Mkinen, Taija" uniqKey="Mkinen T" first="Taija" last="Mkinen">Taija Mkinen</name><name sortKey="Murtomki, Aino" sort="Murtomki, Aino" uniqKey="Murtomki A" first="Aino" last="Murtomki">Aino Murtomki</name><name sortKey="Nurmi, Harri" sort="Nurmi, Harri" uniqKey="Nurmi H" first="Harri" last="Nurmi">Harri Nurmi</name><name sortKey="Tvorogov, Denis" sort="Tvorogov, Denis" uniqKey="Tvorogov D" first="Denis" last="Tvorogov">Denis Tvorogov</name><name sortKey="Yl Herttuala, Seppo" sort="Yl Herttuala, Seppo" uniqKey="Yl Herttuala S" first="Seppo" last="Yl-Herttuala">Seppo Yl-Herttuala</name><name sortKey="Zarkada, Georgia" sort="Zarkada, Georgia" uniqKey="Zarkada G" first="Georgia" last="Zarkada">Georgia Zarkada</name><name sortKey="Zheng, Wei" sort="Zheng, Wei" uniqKey="Zheng W" first="Wei" last="Zheng">Wei Zheng</name></country><country name="Royaume-Uni"><noRegion><name sortKey="Jakobsson, Lars" sort="Jakobsson, Lars" uniqKey="Jakobsson L" first="Lars" last="Jakobsson">Lars Jakobsson</name></noRegion><name sortKey="Franco, Claudio A" sort="Franco, Claudio A" uniqKey="Franco C" first="Claudio A." last="Franco">Claudio A. Franco</name><name sortKey="Fruttiger, Marcus" sort="Fruttiger, Marcus" uniqKey="Fruttiger M" first="Marcus" last="Fruttiger">Marcus Fruttiger</name><name sortKey="Gerhardt, Holger" sort="Gerhardt, Holger" uniqKey="Gerhardt H" first="Holger" last="Gerhardt">Holger Gerhardt</name></country><country name="États-Unis"><noRegion><name sortKey="Aranda, Evelyn" sort="Aranda, Evelyn" uniqKey="Aranda E" first="Evelyn" last="Aranda">Evelyn Aranda</name></noRegion><name sortKey="Pollard, Jeffrey W" sort="Pollard, Jeffrey W" uniqKey="Pollard J" first="Jeffrey W." last="Pollard">Jeffrey W. 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