DLL4 promotes continuous adult intestinal lacteal regeneration and dietary fat transport
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Auteurs : Jeremiah Bernier-Latmani [Suisse] ; Christophe Cisarovsky [Suisse] ; Cansaran Saygili Demir [Suisse] ; Marine Bruand [Suisse] ; Muriel Jaquet [Suisse] ; Suzel Davanture [Suisse] ; Simone Ragusa [Suisse] ; Stefanie Siegert [Suisse] ; Olivier Dormond [Suisse] ; Rui Benedito [Espagne] ; Freddy Radtke [Suisse] ; Sanjiv A. Luther [Suisse] ; Tatiana V. Petrova [Suisse]Source :
- The Journal of Clinical Investigation [ 0021-9738 ] ; ????.
Abstract
The small intestine is a dynamic and complex organ that is characterized by constant epithelium turnover and crosstalk among various cell types and the microbiota. Lymphatic capillaries of the small intestine, called lacteals, play key roles in dietary fat absorption and the gut immune response; however, little is known about the molecular regulation of lacteal function. Here, we performed a high-resolution analysis of the small intestinal stroma and determined that lacteals reside in a permanent regenerative, proliferative state that is distinct from embryonic lymphangiogenesis or quiescent lymphatic vessels observed in other tissues. We further demonstrated that this continuous regeneration process is mediated by Notch signaling and that the expression of the Notch ligand delta-like 4 (DLL4) in lacteals requires activation of VEGFR3 and VEGFR2. Moreover, genetic inactivation of
Url:
DOI: 10.1172/JCI82045
PubMed: 26529256
PubMed Central: 4665794
Affiliations:
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">DLL4 promotes continuous adult intestinal lacteal regeneration and dietary fat transport</title><author><name sortKey="Bernier Latmani, Jeremiah" sort="Bernier Latmani, Jeremiah" uniqKey="Bernier Latmani J" first="Jeremiah" last="Bernier-Latmani">Jeremiah Bernier-Latmani</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de 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uniqKey="Demir C" first="Cansaran Saygili" last="Demir">Cansaran Saygili Demir</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Bruand, Marine" sort="Bruand, Marine" uniqKey="Bruand M" first="Marine" last="Bruand">Marine Bruand</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Jaquet, Muriel" sort="Jaquet, Muriel" uniqKey="Jaquet M" first="Muriel" last="Jaquet">Muriel Jaquet</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Davanture, Suzel" sort="Davanture, Suzel" uniqKey="Davanture S" first="Suzel" last="Davanture">Suzel Davanture</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Ragusa, Simone" sort="Ragusa, Simone" uniqKey="Ragusa S" first="Simone" last="Ragusa">Simone Ragusa</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Siegert, Stefanie" sort="Siegert, Stefanie" uniqKey="Siegert S" first="Stefanie" last="Siegert">Stefanie Siegert</name><affiliation wicri:level="1"><nlm:aff id="A2">Department of Biochemistry, UNIL, Epalinges, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Biochemistry, UNIL, Epalinges</wicri:regionArea><wicri:noRegion>Epalinges</wicri:noRegion></affiliation></author><author><name sortKey="Dormond, Olivier" sort="Dormond, Olivier" uniqKey="Dormond O" first="Olivier" last="Dormond">Olivier Dormond</name><affiliation wicri:level="3"><nlm:aff id="A3">Department of Internal Surgery, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Internal Surgery, CHUV, 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Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Cisarovsky, Christophe" sort="Cisarovsky, Christophe" uniqKey="Cisarovsky C" first="Christophe" last="Cisarovsky">Christophe Cisarovsky</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Demir, Cansaran Saygili" sort="Demir, Cansaran Saygili" uniqKey="Demir C" first="Cansaran Saygili" last="Demir">Cansaran Saygili Demir</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Bruand, Marine" sort="Bruand, Marine" uniqKey="Bruand M" first="Marine" last="Bruand">Marine Bruand</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Jaquet, Muriel" sort="Jaquet, Muriel" uniqKey="Jaquet M" first="Muriel" last="Jaquet">Muriel Jaquet</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Davanture, Suzel" sort="Davanture, Suzel" uniqKey="Davanture S" first="Suzel" last="Davanture">Suzel Davanture</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Ragusa, Simone" sort="Ragusa, Simone" uniqKey="Ragusa S" first="Simone" last="Ragusa">Simone Ragusa</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Siegert, Stefanie" sort="Siegert, Stefanie" uniqKey="Siegert S" first="Stefanie" last="Siegert">Stefanie Siegert</name><affiliation wicri:level="1"><nlm:aff id="A2">Department of Biochemistry, UNIL, Epalinges, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Biochemistry, UNIL, Epalinges</wicri:regionArea><wicri:noRegion>Epalinges</wicri:noRegion></affiliation></author><author><name sortKey="Dormond, Olivier" sort="Dormond, Olivier" uniqKey="Dormond O" first="Olivier" last="Dormond">Olivier Dormond</name><affiliation wicri:level="3"><nlm:aff id="A3">Department of Internal Surgery, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Internal Surgery, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Benedito, Rui" sort="Benedito, Rui" uniqKey="Benedito R" first="Rui" last="Benedito">Rui Benedito</name><affiliation wicri:level="3"><nlm:aff id="A4">Centro Nacional de Investigaciones Cardiovasculares (CNIC), Madrid, Spain.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Espagne</country><wicri:regionArea>Centro Nacional de Investigaciones Cardiovasculares (CNIC), Madrid</wicri:regionArea><placeName><settlement type="city">Madrid</settlement><region nuts="2" type="region">Communauté de Madrid</region></placeName></affiliation></author><author><name sortKey="Radtke, Freddy" sort="Radtke, Freddy" uniqKey="Radtke F" first="Freddy" last="Radtke">Freddy Radtke</name><affiliation wicri:level="3"><nlm:aff id="A5">Swiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology Lausanne (EPFL), Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Swiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology Lausanne (EPFL), Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation></author><author><name sortKey="Luther, Sanjiv A" sort="Luther, Sanjiv A" uniqKey="Luther S" first="Sanjiv A." last="Luther">Sanjiv A. Luther</name><affiliation wicri:level="1"><nlm:aff id="A2">Department of Biochemistry, UNIL, Epalinges, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Biochemistry, UNIL, Epalinges</wicri:regionArea><wicri:noRegion>Epalinges</wicri:noRegion></affiliation></author><author><name sortKey="Petrova, Tatiana V" sort="Petrova, Tatiana V" uniqKey="Petrova T" first="Tatiana V." last="Petrova">Tatiana V. Petrova</name><affiliation wicri:level="3"><nlm:aff id="A1">Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Department of Fundamental Oncology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne (UNIL), and Division of Experimental Pathology, Institute of Pathology, CHUV, Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="A5">Swiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology Lausanne (EPFL), Lausanne, Switzerland.</nlm:aff><country xml:lang="fr" wicri:curation="lc">Suisse</country><wicri:regionArea>Swiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology Lausanne (EPFL), Lausanne</wicri:regionArea><placeName><settlement type="city">Lausanne</settlement><region nuts="3" type="region">Canton de Vaud</region></placeName></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="????">????</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The small intestine is a dynamic and complex organ that is characterized by constant epithelium turnover and crosstalk among various cell types and the microbiota. Lymphatic capillaries of the small intestine, called lacteals, play key roles in dietary fat absorption and the gut immune response; however, little is known about the molecular regulation of lacteal function. Here, we performed a high-resolution analysis of the small intestinal stroma and determined that lacteals reside in a permanent regenerative, proliferative state that is distinct from embryonic lymphangiogenesis or quiescent lymphatic vessels observed in other tissues. We further demonstrated that this continuous regeneration process is mediated by Notch signaling and that the expression of the Notch ligand delta-like 4 (DLL4) in lacteals requires activation of VEGFR3 and VEGFR2. Moreover, genetic inactivation of <italic>Dll4</italic> in lymphatic endothelial cells led to lacteal regression and impaired dietary fat uptake. We propose that such a slow lymphatic regeneration mode is necessary to match a unique need of intestinal lymphatic vessels for both continuous maintenance, due to the constant exposure to dietary fat and mechanical strain, and efficient uptake of fat and immune cells. Our work reveals how lymphatic vessel responses are shaped by tissue specialization and uncover a role for continuous DLL4 signaling in the function of adult lymphatic vasculature.</p></div></front></TEI><affiliations><list><country><li>Espagne</li><li>Suisse</li></country><region><li>Canton de Vaud</li><li>Communauté de Madrid</li></region><settlement><li>Lausanne</li><li>Madrid</li></settlement></list><tree><country name="Suisse"><region name="Canton de Vaud"><name sortKey="Bernier Latmani, Jeremiah" sort="Bernier Latmani, Jeremiah" uniqKey="Bernier Latmani J" first="Jeremiah" last="Bernier-Latmani">Jeremiah Bernier-Latmani</name></region><name sortKey="Bruand, Marine" sort="Bruand, Marine" uniqKey="Bruand M" first="Marine" last="Bruand">Marine Bruand</name><name sortKey="Cisarovsky, Christophe" sort="Cisarovsky, Christophe" uniqKey="Cisarovsky C" first="Christophe" last="Cisarovsky">Christophe Cisarovsky</name><name sortKey="Davanture, Suzel" sort="Davanture, Suzel" uniqKey="Davanture S" first="Suzel" last="Davanture">Suzel Davanture</name><name sortKey="Demir, Cansaran Saygili" sort="Demir, Cansaran Saygili" uniqKey="Demir C" first="Cansaran Saygili" last="Demir">Cansaran Saygili Demir</name><name sortKey="Dormond, Olivier" sort="Dormond, Olivier" uniqKey="Dormond O" first="Olivier" last="Dormond">Olivier Dormond</name><name sortKey="Jaquet, Muriel" sort="Jaquet, Muriel" uniqKey="Jaquet M" first="Muriel" last="Jaquet">Muriel Jaquet</name><name sortKey="Luther, Sanjiv A" sort="Luther, Sanjiv A" uniqKey="Luther S" first="Sanjiv A." last="Luther">Sanjiv A. Luther</name><name sortKey="Petrova, Tatiana V" sort="Petrova, Tatiana V" uniqKey="Petrova T" first="Tatiana V." last="Petrova">Tatiana V. Petrova</name><name sortKey="Petrova, Tatiana V" sort="Petrova, Tatiana V" uniqKey="Petrova T" first="Tatiana V." last="Petrova">Tatiana V. Petrova</name><name sortKey="Radtke, Freddy" sort="Radtke, Freddy" uniqKey="Radtke F" first="Freddy" last="Radtke">Freddy Radtke</name><name sortKey="Ragusa, Simone" sort="Ragusa, Simone" uniqKey="Ragusa S" first="Simone" last="Ragusa">Simone Ragusa</name><name sortKey="Siegert, Stefanie" sort="Siegert, Stefanie" uniqKey="Siegert S" first="Stefanie" last="Siegert">Stefanie Siegert</name></country><country name="Espagne"><region name="Communauté de Madrid"><name sortKey="Benedito, Rui" sort="Benedito, Rui" uniqKey="Benedito R" first="Rui" last="Benedito">Rui Benedito</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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