Matrix metalloproteinase-2 governs lymphatic vessel formation as an interstitial collagenase.
Identifieur interne : 004133 ( Main/Exploration ); précédent : 004132; suivant : 004134Matrix metalloproteinase-2 governs lymphatic vessel formation as an interstitial collagenase.
Auteurs : Benoit Detry [Belgique] ; Charlotte Erpicum ; Jenny Paupert ; Silvia Blacher ; Catherine Maillard ; Françoise Bruyère ; Hélène Pendeville ; Thibault Remacle ; Vincent Lambert ; Cédric Balsat ; Sandra Ormenese ; Françoise Lamaye ; Els Janssens ; Lieve Moons ; Didier Cataldo ; Frédéric Kridelka ; Peter Carmeliet ; Marc Thiry ; Jean-Michel Foidart ; Ingrid Struman ; Agnès NoëlSource :
- Blood [ 1528-0020 ] ; 2012.
Descripteurs français
- KwdFr :
- Animal génétiquement modifié, Animaux, Cellules cultivées, Collagenases (génétique), Collagenases (métabolisme), Collagenases (physiologie), Collagène de type I (métabolisme), Danio zébré, Embryon non mammalien, Femelle, Humains, Liquide extracellulaire (enzymologie), Liquide extracellulaire (métabolisme), Lymphangiogenèse (génétique), Matrix metalloproteinase 2 (génétique), Matrix metalloproteinase 2 (métabolisme), Matrix metalloproteinase 2 (physiologie), Mâle, Souris, Souris de lignée C57BL, Souris knockout, Vaisseaux lymphatiques (embryologie), Vaisseaux lymphatiques (métabolisme), Vaisseaux lymphatiques (physiologie).
- MESH :
- embryologie : Vaisseaux lymphatiques.
- enzymologie : Liquide extracellulaire.
- génétique : Collagenases, Lymphangiogenèse, Matrix metalloproteinase 2.
- métabolisme : Collagenases, Collagène de type I, Liquide extracellulaire, Matrix metalloproteinase 2, Vaisseaux lymphatiques.
- physiologie : Collagenases, Matrix metalloproteinase 2, Vaisseaux lymphatiques.
- Animal génétiquement modifié, Animaux, Cellules cultivées, Danio zébré, Embryon non mammalien, Femelle, Humains, Mâle, Souris, Souris de lignée C57BL, Souris knockout.
English descriptors
- KwdEn :
- Animals, Animals, Genetically Modified, Cells, Cultured, Collagen Type I (metabolism), Collagenases (genetics), Collagenases (metabolism), Collagenases (physiology), Embryo, Nonmammalian, Extracellular Fluid (enzymology), Extracellular Fluid (metabolism), Female, Humans, Lymphangiogenesis (genetics), Lymphatic Vessels (embryology), Lymphatic Vessels (metabolism), Lymphatic Vessels (physiology), Male, Matrix Metalloproteinase 2 (genetics), Matrix Metalloproteinase 2 (metabolism), Matrix Metalloproteinase 2 (physiology), Mice, Mice, Inbred C57BL, Mice, Knockout, Zebrafish.
- MESH :
- chemical , genetics : Collagenases, Matrix Metalloproteinase 2.
- chemical , metabolism : Collagen Type I, Collagenases, Matrix Metalloproteinase 2.
- chemical , physiology : Collagenases, Matrix Metalloproteinase 2.
- embryology : Lymphatic Vessels.
- enzymology : Extracellular Fluid.
- genetics : Lymphangiogenesis.
- metabolism : Extracellular Fluid, Lymphatic Vessels.
- physiology : Lymphatic Vessels.
- Animals, Animals, Genetically Modified, Cells, Cultured, Embryo, Nonmammalian, Female, Humans, Male, Mice, Mice, Inbred C57BL, Mice, Knockout, Zebrafish.
Abstract
Lymphatic dysfunctions are associated with several human diseases, including lymphedema and metastatic spread of cancer. Although it is well recognized that lymphatic capillaries attach directly to interstitial matrix mainly composed of fibrillar type I collagen, the interactions occurring between lymphatics and their surrounding matrix have been overlooked. In this study, we demonstrate how matrix metalloproteinase (MMP)-2 drives lymphatic morphogenesis through Mmp2-gene ablation in mice, mmp2 knockdown in zebrafish and in 3D-culture systems, and through MMP2 inhibition. In all models used in vivo (3 murine models and thoracic duct development in zebrafish) and in vitro (lymphatic ring and spheroid assays), MMP2 blockage or down-regulation leads to reduced lymphangiogenesis or altered vessel branching. Our data show that lymphatic endothelial cell (LEC) migration through collagen fibers is affected by physical matrix constraints (matrix composition, density, and cross-linking). Transmission electron microscopy and confocal reflection microscopy using DQ-collagen highlight the contribution of MMP2 to mesenchymal-like migration of LECs associated with collagen fiber remodeling. Our findings provide new mechanistic insight into how LECs negotiate an interstitial type I collagen barrier and reveal an unexpected MMP2-driven collagenolytic pathway for lymphatic vessel formation and morphogenesis.
DOI: 10.1182/blood-2011-12-400267
PubMed: 22490679
Affiliations:
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Le document en format XML
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xml:lang="en">Matrix metalloproteinase-2 governs lymphatic vessel formation as an interstitial collagenase.</title><author><name sortKey="Detry, Benoit" sort="Detry, Benoit" uniqKey="Detry B" first="Benoit" last="Detry">Benoit Detry</name><affiliation wicri:level="4"><nlm:affiliation>Laboratory of Tumor and Development Biology, Groupe Interdisciplinaire de Génoprotéomique Appliqué-Recherche (GIGA-Cancer), University of Liège, Liège, Belgium;</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Laboratory of Tumor and Development Biology, Groupe Interdisciplinaire de Génoprotéomique Appliqué-Recherche (GIGA-Cancer), University of Liège, Liège</wicri:regionArea><orgName type="university">Université de Liège</orgName><placeName><settlement type="city">Liège</settlement><region type="region" nuts="1">Région wallonne</region><region type="province" nuts="1">Province de Liège</region></placeName></affiliation></author><author><name sortKey="Erpicum, Charlotte" sort="Erpicum, Charlotte" uniqKey="Erpicum C" first="Charlotte" last="Erpicum">Charlotte Erpicum</name></author><author><name sortKey="Paupert, Jenny" sort="Paupert, Jenny" uniqKey="Paupert J" first="Jenny" last="Paupert">Jenny Paupert</name></author><author><name sortKey="Blacher, Silvia" sort="Blacher, Silvia" uniqKey="Blacher S" first="Silvia" last="Blacher">Silvia Blacher</name></author><author><name sortKey="Maillard, Catherine" sort="Maillard, Catherine" uniqKey="Maillard C" first="Catherine" last="Maillard">Catherine Maillard</name></author><author><name sortKey="Bruyere, Francoise" sort="Bruyere, Francoise" uniqKey="Bruyere F" first="Françoise" last="Bruyère">Françoise Bruyère</name></author><author><name sortKey="Pendeville, Helene" sort="Pendeville, Helene" uniqKey="Pendeville H" first="Hélène" last="Pendeville">Hélène Pendeville</name></author><author><name sortKey="Remacle, Thibault" sort="Remacle, Thibault" uniqKey="Remacle T" first="Thibault" last="Remacle">Thibault Remacle</name></author><author><name sortKey="Lambert, Vincent" sort="Lambert, Vincent" uniqKey="Lambert V" first="Vincent" last="Lambert">Vincent Lambert</name></author><author><name sortKey="Balsat, Cedric" sort="Balsat, Cedric" uniqKey="Balsat C" first="Cédric" last="Balsat">Cédric Balsat</name></author><author><name sortKey="Ormenese, Sandra" sort="Ormenese, Sandra" uniqKey="Ormenese S" first="Sandra" last="Ormenese">Sandra Ormenese</name></author><author><name sortKey="Lamaye, Francoise" sort="Lamaye, Francoise" uniqKey="Lamaye F" first="Françoise" last="Lamaye">Françoise Lamaye</name></author><author><name sortKey="Janssens, Els" sort="Janssens, Els" uniqKey="Janssens E" first="Els" last="Janssens">Els Janssens</name></author><author><name sortKey="Moons, Lieve" sort="Moons, Lieve" uniqKey="Moons L" first="Lieve" last="Moons">Lieve Moons</name></author><author><name sortKey="Cataldo, Didier" sort="Cataldo, Didier" uniqKey="Cataldo D" first="Didier" last="Cataldo">Didier Cataldo</name></author><author><name sortKey="Kridelka, Frederic" sort="Kridelka, Frederic" uniqKey="Kridelka F" first="Frédéric" last="Kridelka">Frédéric Kridelka</name></author><author><name sortKey="Carmeliet, Peter" sort="Carmeliet, Peter" uniqKey="Carmeliet P" first="Peter" last="Carmeliet">Peter Carmeliet</name></author><author><name sortKey="Thiry, Marc" sort="Thiry, Marc" uniqKey="Thiry M" first="Marc" last="Thiry">Marc Thiry</name></author><author><name sortKey="Foidart, Jean Michel" sort="Foidart, Jean Michel" uniqKey="Foidart J" first="Jean-Michel" last="Foidart">Jean-Michel Foidart</name></author><author><name sortKey="Struman, Ingrid" sort="Struman, Ingrid" uniqKey="Struman I" first="Ingrid" last="Struman">Ingrid Struman</name></author><author><name sortKey="Noel, Agnes" sort="Noel, Agnes" uniqKey="Noel A" first="Agnès" last="Noël">Agnès Noël</name></author></analytic><series><title level="j">Blood</title><idno type="eISSN">1528-0020</idno><imprint><date when="2012" type="published">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Animals, Genetically Modified</term><term>Cells, Cultured</term><term>Collagen Type I (metabolism)</term><term>Collagenases (genetics)</term><term>Collagenases (metabolism)</term><term>Collagenases (physiology)</term><term>Embryo, Nonmammalian</term><term>Extracellular Fluid (enzymology)</term><term>Extracellular Fluid (metabolism)</term><term>Female</term><term>Humans</term><term>Lymphangiogenesis (genetics)</term><term>Lymphatic Vessels (embryology)</term><term>Lymphatic Vessels (metabolism)</term><term>Lymphatic Vessels (physiology)</term><term>Male</term><term>Matrix Metalloproteinase 2 (genetics)</term><term>Matrix Metalloproteinase 2 (metabolism)</term><term>Matrix Metalloproteinase 2 (physiology)</term><term>Mice</term><term>Mice, Inbred C57BL</term><term>Mice, Knockout</term><term>Zebrafish</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Animal génétiquement modifié</term><term>Animaux</term><term>Cellules cultivées</term><term>Collagenases (génétique)</term><term>Collagenases (métabolisme)</term><term>Collagenases (physiologie)</term><term>Collagène de type I (métabolisme)</term><term>Danio zébré</term><term>Embryon non mammalien</term><term>Femelle</term><term>Humains</term><term>Liquide extracellulaire (enzymologie)</term><term>Liquide extracellulaire (métabolisme)</term><term>Lymphangiogenèse (génétique)</term><term>Matrix metalloproteinase 2 (génétique)</term><term>Matrix metalloproteinase 2 (métabolisme)</term><term>Matrix metalloproteinase 2 (physiologie)</term><term>Mâle</term><term>Souris</term><term>Souris de lignée C57BL</term><term>Souris knockout</term><term>Vaisseaux lymphatiques (embryologie)</term><term>Vaisseaux lymphatiques (métabolisme)</term><term>Vaisseaux lymphatiques (physiologie)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Collagenases</term><term>Matrix Metalloproteinase 2</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Collagen Type I</term><term>Collagenases</term><term>Matrix Metalloproteinase 2</term></keywords><keywords scheme="MESH" type="chemical" qualifier="physiology" xml:lang="en"><term>Collagenases</term><term>Matrix Metalloproteinase 2</term></keywords><keywords scheme="MESH" qualifier="embryologie" xml:lang="fr"><term>Vaisseaux lymphatiques</term></keywords><keywords scheme="MESH" qualifier="embryology" xml:lang="en"><term>Lymphatic Vessels</term></keywords><keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr"><term>Liquide extracellulaire</term></keywords><keywords scheme="MESH" qualifier="enzymology" xml:lang="en"><term>Extracellular Fluid</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Lymphangiogenesis</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Collagenases</term><term>Lymphangiogenèse</term><term>Matrix metalloproteinase 2</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Extracellular Fluid</term><term>Lymphatic Vessels</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Collagenases</term><term>Collagène de type I</term><term>Liquide extracellulaire</term><term>Matrix metalloproteinase 2</term><term>Vaisseaux lymphatiques</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Collagenases</term><term>Matrix metalloproteinase 2</term><term>Vaisseaux lymphatiques</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Lymphatic Vessels</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Animals, Genetically Modified</term><term>Cells, Cultured</term><term>Embryo, Nonmammalian</term><term>Female</term><term>Humans</term><term>Male</term><term>Mice</term><term>Mice, Inbred C57BL</term><term>Mice, Knockout</term><term>Zebrafish</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animal génétiquement modifié</term><term>Animaux</term><term>Cellules cultivées</term><term>Danio zébré</term><term>Embryon non mammalien</term><term>Femelle</term><term>Humains</term><term>Mâle</term><term>Souris</term><term>Souris de lignée C57BL</term><term>Souris knockout</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Lymphatic dysfunctions are associated with several human diseases, including lymphedema and metastatic spread of cancer. Although it is well recognized that lymphatic capillaries attach directly to interstitial matrix mainly composed of fibrillar type I collagen, the interactions occurring between lymphatics and their surrounding matrix have been overlooked. In this study, we demonstrate how matrix metalloproteinase (MMP)-2 drives lymphatic morphogenesis through Mmp2-gene ablation in mice, mmp2 knockdown in zebrafish and in 3D-culture systems, and through MMP2 inhibition. In all models used in vivo (3 murine models and thoracic duct development in zebrafish) and in vitro (lymphatic ring and spheroid assays), MMP2 blockage or down-regulation leads to reduced lymphangiogenesis or altered vessel branching. Our data show that lymphatic endothelial cell (LEC) migration through collagen fibers is affected by physical matrix constraints (matrix composition, density, and cross-linking). Transmission electron microscopy and confocal reflection microscopy using DQ-collagen highlight the contribution of MMP2 to mesenchymal-like migration of LECs associated with collagen fiber remodeling. Our findings provide new mechanistic insight into how LECs negotiate an interstitial type I collagen barrier and reveal an unexpected MMP2-driven collagenolytic pathway for lymphatic vessel formation and morphogenesis.</div></front></TEI><affiliations><list><country><li>Belgique</li></country><region><li>Province de Liège</li><li>Région wallonne</li></region><settlement><li>Liège</li></settlement><orgName><li>Université de Liège</li></orgName></list><tree><noCountry><name sortKey="Balsat, Cedric" sort="Balsat, Cedric" uniqKey="Balsat C" first="Cédric" last="Balsat">Cédric Balsat</name><name sortKey="Blacher, Silvia" sort="Blacher, Silvia" uniqKey="Blacher S" first="Silvia" last="Blacher">Silvia Blacher</name><name sortKey="Bruyere, Francoise" sort="Bruyere, Francoise" uniqKey="Bruyere F" first="Françoise" last="Bruyère">Françoise Bruyère</name><name sortKey="Carmeliet, Peter" sort="Carmeliet, Peter" uniqKey="Carmeliet P" first="Peter" last="Carmeliet">Peter Carmeliet</name><name sortKey="Cataldo, Didier" sort="Cataldo, Didier" uniqKey="Cataldo D" first="Didier" last="Cataldo">Didier Cataldo</name><name sortKey="Erpicum, Charlotte" sort="Erpicum, Charlotte" uniqKey="Erpicum C" first="Charlotte" last="Erpicum">Charlotte Erpicum</name><name sortKey="Foidart, Jean Michel" sort="Foidart, Jean Michel" uniqKey="Foidart J" first="Jean-Michel" last="Foidart">Jean-Michel Foidart</name><name sortKey="Janssens, Els" sort="Janssens, Els" uniqKey="Janssens E" first="Els" last="Janssens">Els Janssens</name><name sortKey="Kridelka, Frederic" sort="Kridelka, Frederic" uniqKey="Kridelka F" first="Frédéric" last="Kridelka">Frédéric Kridelka</name><name sortKey="Lamaye, Francoise" sort="Lamaye, Francoise" uniqKey="Lamaye F" first="Françoise" last="Lamaye">Françoise Lamaye</name><name sortKey="Lambert, Vincent" sort="Lambert, Vincent" uniqKey="Lambert V" first="Vincent" last="Lambert">Vincent Lambert</name><name sortKey="Maillard, Catherine" sort="Maillard, Catherine" uniqKey="Maillard C" first="Catherine" last="Maillard">Catherine Maillard</name><name sortKey="Moons, Lieve" sort="Moons, Lieve" uniqKey="Moons L" first="Lieve" last="Moons">Lieve Moons</name><name sortKey="Noel, Agnes" sort="Noel, Agnes" uniqKey="Noel A" first="Agnès" last="Noël">Agnès Noël</name><name sortKey="Ormenese, Sandra" sort="Ormenese, Sandra" uniqKey="Ormenese S" first="Sandra" last="Ormenese">Sandra Ormenese</name><name sortKey="Paupert, Jenny" sort="Paupert, Jenny" uniqKey="Paupert J" first="Jenny" last="Paupert">Jenny Paupert</name><name sortKey="Pendeville, Helene" sort="Pendeville, Helene" uniqKey="Pendeville H" first="Hélène" last="Pendeville">Hélène Pendeville</name><name sortKey="Remacle, Thibault" sort="Remacle, Thibault" uniqKey="Remacle T" first="Thibault" last="Remacle">Thibault Remacle</name><name sortKey="Struman, Ingrid" sort="Struman, Ingrid" uniqKey="Struman I" first="Ingrid" last="Struman">Ingrid Struman</name><name sortKey="Thiry, Marc" sort="Thiry, Marc" uniqKey="Thiry M" first="Marc" last="Thiry">Marc Thiry</name></noCountry><country name="Belgique"><region name="Région wallonne"><name sortKey="Detry, Benoit" sort="Detry, Benoit" uniqKey="Detry B" first="Benoit" last="Detry">Benoit Detry</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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