VEGF-C–dependent stimulation of lymphatic function ameliorates experimental inflammatory bowel disease
Identifieur interne : 000104 ( France/Analysis ); précédent : 000103; suivant : 000105VEGF-C–dependent stimulation of lymphatic function ameliorates experimental inflammatory bowel disease
Auteurs : Silvia D Lessio [Italie] ; Carmen Correale [Italie] ; Carlotta Tacconi [Italie] ; Alessandro Gandelli [Italie] ; Giovanni Pietrogrande [Italie] ; Stefania Vetrano [Italie] ; Marco Genua [Italie] ; Vincenzo Arena [Italie] ; Antonino Spinelli [Italie] ; Laurent Peyrin-Biroulet [France] ; Claudio Fiocchi [États-Unis] ; Silvio Danese [Italie]Source :
- The Journal of Clinical Investigation [ 0021-9738 ] ; 2014.
Abstract
Crohn’s disease (CD) and ulcerative colitis (UC) are chronic inflammatory bowel diseases (IBDs) of unknown etiology that are associated with an aberrant mucosal immune response. Neoangiogenesis and vascular injury are observed in IBD along with increased lymphangiogenesis. While the pathogenic role of angiogenesis in IBD is well characterized, it is not clear how or if increased lymphangiogenesis promotes disease. Here, we determined that enhancing lymphangiogenesis and lymphatic function reduces experimental IBD. Specifically, we demonstrated that adenoviral induction of prolymphangiogenic factor VEGF-C provides marked protection against the development of acute and chronic colitis in 2 different animal models. VEGF-C–dependent protection was observed in combination with increased inflammatory cell mobilization and bacterial antigen clearance from the inflamed colon to the draining lymph nodes. Moreover, we found that the VEGF-C/VEGFR3 pathway regulates macrophage (MΦ) plasticity and activation both in cultured MΦs and in vivo, imparting a hybrid M1-M2 phenotype. The protective function of VEGF-C was meditated by the so-called resolving MΦs during chronic experimental colitis in a STAT6-dependent manner. Together, these findings shed light on the contribution of lymphatics to the pathogenesis of gut inflammation and suggest that correction of defective lymphatic function with VEGF-C has potential as a therapeutic strategy for IBD.
Url:
DOI: 10.1172/JCI72189
PubMed: 25105363
PubMed Central: 4151217
Affiliations:
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Rozzano</wicri:regionArea><wicri:noRegion>Rozzano</wicri:noRegion></affiliation></author><author><name sortKey="Pietrogrande, Giovanni" sort="Pietrogrande, Giovanni" uniqKey="Pietrogrande G" first="Giovanni" last="Pietrogrande">Giovanni Pietrogrande</name><affiliation wicri:level="3"><nlm:aff id="JCI72189">Center for Translational Genomics and Bioinformatics, San Raffaele University and Scientific Institute, Milan, Italy.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Italie</country><wicri:regionArea>Center for Translational Genomics and Bioinformatics, San Raffaele University and Scientific Institute, Milan</wicri:regionArea><placeName><settlement type="city">Milan</settlement><region nuts="2">Lombardie</region></placeName></affiliation></author><author><name sortKey="Vetrano, Stefania" sort="Vetrano, Stefania" uniqKey="Vetrano S" first="Stefania" last="Vetrano">Stefania Vetrano</name><affiliation wicri:level="1"><nlm:aff id="JCI72189">IBD Center, Department of Gastroenterology, 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wicri:level="3"><nlm:aff id="JCI72189">Institute of Pathology, Catholic University of the Sacred Heart, Rome, Italy.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Italie</country><wicri:regionArea>Institute of Pathology, Catholic University of the Sacred Heart, Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Spinelli, Antonino" sort="Spinelli, Antonino" uniqKey="Spinelli A" first="Antonino" last="Spinelli">Antonino Spinelli</name><affiliation wicri:level="1"><nlm:aff id="JCI72189">IBD Center, Department of Gastroenterology, Humanitas Clinical and Research Center, Rozzano, Italy.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Italie</country><wicri:regionArea>IBD Center, Department of Gastroenterology, Humanitas Clinical and Research Center, Rozzano</wicri:regionArea><wicri:noRegion>Rozzano</wicri:noRegion></affiliation></author><author><name sortKey="Peyrin Biroulet, Laurent" sort="Peyrin Biroulet, Laurent" uniqKey="Peyrin Biroulet L" first="Laurent" last="Peyrin-Biroulet">Laurent Peyrin-Biroulet</name><affiliation wicri:level="3"><nlm:aff id="JCI72189">Department of Hepato-Gastroenterology, University Hospital of Nancy, Nancy, France.</nlm:aff><country xml:lang="fr" wicri:curation="lc">France</country><wicri:regionArea>Department of Hepato-Gastroenterology, University Hospital of Nancy, Nancy</wicri:regionArea><placeName><region type="region">Grand Est</region><region type="old region">Lorraine (région)</region><settlement type="city">Nancy</settlement></placeName></affiliation></author><author><name sortKey="Fiocchi, Claudio" sort="Fiocchi, Claudio" uniqKey="Fiocchi C" first="Claudio" last="Fiocchi">Claudio Fiocchi</name><affiliation><nlm:aff wicri:cut=", and" id="JCI72189">Department of Gastroenterology and Hepatology, Digestive Disease Institute</nlm:aff><wicri:noCountry code="subfield">Digestive Disease Institute</wicri:noCountry></affiliation><affiliation wicri:level="2"><nlm:aff id="JCI72189">Department of Pathobiology, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, Ohio, USA.</nlm:aff><country xml:lang="fr" wicri:curation="lc">États-Unis</country><wicri:regionArea>Department of Pathobiology, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, Ohio</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Danese, Silvio" sort="Danese, Silvio" uniqKey="Danese S" first="Silvio" last="Danese">Silvio Danese</name><affiliation wicri:level="1"><nlm:aff id="JCI72189">IBD Center, Department of Gastroenterology, Humanitas Clinical and Research Center, Rozzano, Italy.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Italie</country><wicri:regionArea>IBD Center, Department of Gastroenterology, Humanitas Clinical and Research Center, Rozzano</wicri:regionArea><wicri:noRegion>Rozzano</wicri:noRegion></affiliation></author></analytic><series><title level="j">The Journal of Clinical Investigation</title><idno type="ISSN">0021-9738</idno><idno type="eISSN">1558-8238</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Crohn’s disease (CD) and ulcerative colitis (UC) are chronic inflammatory bowel diseases (IBDs) of unknown etiology that are associated with an aberrant mucosal immune response. Neoangiogenesis and vascular injury are observed in IBD along with increased lymphangiogenesis. While the pathogenic role of angiogenesis in IBD is well characterized, it is not clear how or if increased lymphangiogenesis promotes disease. Here, we determined that enhancing lymphangiogenesis and lymphatic function reduces experimental IBD. Specifically, we demonstrated that adenoviral induction of prolymphangiogenic factor VEGF-C provides marked protection against the development of acute and chronic colitis in 2 different animal models. VEGF-C–dependent protection was observed in combination with increased inflammatory cell mobilization and bacterial antigen clearance from the inflamed colon to the draining lymph nodes. Moreover, we found that the VEGF-C/VEGFR3 pathway regulates macrophage (MΦ) plasticity and activation both in cultured MΦs and in vivo, imparting a hybrid M1-M2 phenotype. The protective function of VEGF-C was meditated by the so-called resolving MΦs during chronic experimental colitis in a STAT6-dependent manner. Together, these findings shed light on the contribution of lymphatics to the pathogenesis of gut inflammation and suggest that correction of defective lymphatic function with VEGF-C has potential as a therapeutic strategy for IBD.</p></div></front></TEI><affiliations><list><country><li>France</li><li>Italie</li><li>États-Unis</li></country><region><li>Grand Est</li><li>Latium</li><li>Lombardie</li><li>Lorraine (région)</li><li>Ohio</li></region><settlement><li>Milan</li><li>Nancy</li><li>Rome</li></settlement></list><tree><country name="Italie"><noRegion><name sortKey="D Lessio, Silvia" sort="D Lessio, Silvia" uniqKey="D Lessio S" first="Silvia" last="D Lessio">Silvia D Lessio</name></noRegion><name sortKey="Arena, Vincenzo" sort="Arena, Vincenzo" uniqKey="Arena V" first="Vincenzo" last="Arena">Vincenzo Arena</name><name sortKey="Correale, Carmen" sort="Correale, Carmen" uniqKey="Correale C" first="Carmen" last="Correale">Carmen Correale</name><name sortKey="Danese, Silvio" sort="Danese, Silvio" uniqKey="Danese S" first="Silvio" last="Danese">Silvio Danese</name><name sortKey="Gandelli, Alessandro" sort="Gandelli, Alessandro" uniqKey="Gandelli A" first="Alessandro" last="Gandelli">Alessandro Gandelli</name><name sortKey="Genua, Marco" sort="Genua, Marco" uniqKey="Genua M" first="Marco" last="Genua">Marco Genua</name><name sortKey="Pietrogrande, Giovanni" sort="Pietrogrande, Giovanni" uniqKey="Pietrogrande G" first="Giovanni" last="Pietrogrande">Giovanni Pietrogrande</name><name sortKey="Spinelli, Antonino" sort="Spinelli, Antonino" uniqKey="Spinelli A" first="Antonino" last="Spinelli">Antonino Spinelli</name><name sortKey="Tacconi, Carlotta" sort="Tacconi, Carlotta" uniqKey="Tacconi C" first="Carlotta" last="Tacconi">Carlotta Tacconi</name><name sortKey="Vetrano, Stefania" sort="Vetrano, Stefania" uniqKey="Vetrano S" first="Stefania" last="Vetrano">Stefania Vetrano</name></country><country name="France"><region name="Grand Est"><name sortKey="Peyrin Biroulet, Laurent" sort="Peyrin Biroulet, Laurent" uniqKey="Peyrin Biroulet L" first="Laurent" last="Peyrin-Biroulet">Laurent Peyrin-Biroulet</name></region></country><country name="États-Unis"><region name="Ohio"><name sortKey="Fiocchi, Claudio" sort="Fiocchi, Claudio" uniqKey="Fiocchi C" first="Claudio" last="Fiocchi">Claudio Fiocchi</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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