Dermal Collagen and Lipid Deposition Correlate with Tissue Swelling and Hydraulic Conductivity in Murine Primary Lymphedema
Identifieur interne : 003895 ( Ncbi/Merge ); précédent : 003894; suivant : 003896Dermal Collagen and Lipid Deposition Correlate with Tissue Swelling and Hydraulic Conductivity in Murine Primary Lymphedema
Auteurs : Joseph M. Rutkowski [Suisse] ; Carl Erik Markhus [Norvège] ; Christina C. Gyenge [Norvège] ; Kari Alitalo [Finlande] ; Helge Wiig [Norvège] ; Melody A. Swartz [Suisse]Source :
- The American Journal of Pathology [ 0002-9440 ] ; 2010.
Descripteurs français
- KwdFr :
- Animaux, Collagène (métabolisme), Derme (anatomopathologie), Derme (métabolisme), Derme (physiopathologie), Femelle, Humains, Liquide extracellulaire (métabolisme), Lymphoedème (anatomopathologie), Lymphoedème (métabolisme), Lymphoedème (physiopathologie), Modèles animaux de maladie humaine, Mâle, Métabolisme des lipides, Phénomènes biomécaniques, Phénotype, Pression, Récepteur-3 au facteur croissance endothéliale vasculaire (métabolisme), Souris, Souris de lignée C57BL.
- MESH :
- anatomopathologie : Derme, Lymphoedème.
- métabolisme : Collagène, Derme, Liquide extracellulaire, Lymphoedème, Récepteur-3 au facteur croissance endothéliale vasculaire.
- physiopathologie : Derme, Lymphoedème.
- Animaux, Femelle, Humains, Modèles animaux de maladie humaine, Mâle, Métabolisme des lipides, Phénomènes biomécaniques, Phénotype, Pression, Souris, Souris de lignée C57BL.
English descriptors
- KwdEn :
- Animals, Biomechanical Phenomena, Collagen (metabolism), Dermis (metabolism), Dermis (pathology), Dermis (physiopathology), Disease Models, Animal, Extracellular Fluid (metabolism), Female, Humans, Lipid Metabolism, Lymphedema (metabolism), Lymphedema (pathology), Lymphedema (physiopathology), Male, Mice, Mice, Inbred C57BL, Phenotype, Pressure, Vascular Endothelial Growth Factor Receptor-3 (metabolism).
- MESH :
- chemical , metabolism : Collagen, Vascular Endothelial Growth Factor Receptor-3.
- metabolism : Dermis, Extracellular Fluid, Lymphedema.
- pathology : Dermis, Lymphedema.
- physiopathology : Dermis, Lymphedema.
- Animals, Biomechanical Phenomena, Disease Models, Animal, Female, Humans, Lipid Metabolism, Male, Mice, Mice, Inbred C57BL, Phenotype, Pressure.
Abstract
Primary lymphedema is a congenital pathology of dysfunctional lymphatic drainage characterized by swelling of the limbs, thickening of the dermis, and fluid and lipid accumulation in the underlying tissue. Two mouse models of primary lymphedema, the Chy mouse and the K14-VEGFR-3-Ig mouse, both lack dermal lymphatic capillaries and exhibit a lymphedematous phenotype attributable to disrupted VEGFR-3 signaling. Here we show that the differences in edematous tissue composition between these two models correlated with drastic differences in hydraulic conductivity. The skin of Chy mice possessed significantly higher levels of collagen and fat, whereas K14-VEGFR-3-Ig mouse skin composition was relatively normal, as compared with their respective wild-type controls. Functionally, this resulted in a greatly increased dermal hydraulic conductivity in K14-VEGFR3-Ig, but not Chy, mice. Our data suggest that lymphedema associated with increased collagen and lipid accumulation counteracts an increased hydraulic conductivity associated with dermal swelling, which in turn further limits interstitial transport and swelling. Without lipid and collagen accumulation, hydraulic conductivity is increased and overall swelling is minimized. These opposing tissue responses to primary lymphedema imply that tissue remodeling—predominantly collagen and fat deposition—may dictate tissue swelling and govern interstitial transport in lymphedema.
Url:
DOI: 10.2353/ajpath.2010.090733
PubMed: 20110415
PubMed Central: 2832135
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<term>Dermis (pathology)</term>
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<term>Derme (métabolisme)</term>
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<term>Lymphoedème</term>
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<term>Lymphedema</term>
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<front><div type="abstract" xml:lang="en"><p>Primary lymphedema is a congenital pathology of dysfunctional lymphatic drainage characterized by swelling of the limbs, thickening of the dermis, and fluid and lipid accumulation in the underlying tissue. Two mouse models of primary lymphedema, the Chy mouse and the K14-VEGFR-3-Ig mouse, both lack dermal lymphatic capillaries and exhibit a lymphedematous phenotype attributable to disrupted VEGFR-3 signaling. Here we show that the differences in edematous tissue composition between these two models correlated with drastic differences in hydraulic conductivity. The skin of Chy mice possessed significantly higher levels of collagen and fat, whereas K14-VEGFR-3-Ig mouse skin composition was relatively normal, as compared with their respective wild-type controls. Functionally, this resulted in a greatly increased dermal hydraulic conductivity in K14-VEGFR3-Ig, but not Chy, mice. Our data suggest that lymphedema associated with increased collagen and lipid accumulation counteracts an increased hydraulic conductivity associated with dermal swelling, which in turn further limits interstitial transport and swelling. Without lipid and collagen accumulation, hydraulic conductivity is increased and overall swelling is minimized. These opposing tissue responses to primary lymphedema imply that tissue remodeling—predominantly collagen and fat deposition—may dictate tissue swelling and govern interstitial transport in lymphedema.</p>
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<author><name sortKey="Gyenge, Christina C" sort="Gyenge, Christina C" uniqKey="Gyenge C" first="Christina C." last="Gyenge">Christina C. Gyenge</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">Department of Biomedicine, University of Bergen, Bergen, Norway</nlm:aff>
<country xml:lang="fr">Norvège</country>
<wicri:regionArea>Department of Biomedicine, University of Bergen, Bergen</wicri:regionArea>
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<author><name sortKey="Alitalo, Kari" sort="Alitalo, Kari" uniqKey="Alitalo K" first="Kari" last="Alitalo">Kari Alitalo</name>
<affiliation wicri:level="1"><nlm:aff id="aff3">Department of Molecular Cancer Biology, Haartman Institute, and Helsinki University Hospital, University of Helsinki, Helsinki, Finland</nlm:aff>
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<wicri:regionArea>Department of Molecular Cancer Biology, Haartman Institute, and Helsinki University Hospital, University of Helsinki, Helsinki</wicri:regionArea>
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<placeName><settlement type="city">Helsinki</settlement>
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<author><name sortKey="Wiig, Helge" sort="Wiig, Helge" uniqKey="Wiig H" first="Helge" last="Wiig">Helge Wiig</name>
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<country xml:lang="fr">Norvège</country>
<wicri:regionArea>Department of Biomedicine, University of Bergen, Bergen</wicri:regionArea>
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<author><name sortKey="Swartz, Melody A" sort="Swartz, Melody A" uniqKey="Swartz M" first="Melody A." last="Swartz">Melody A. Swartz</name>
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<series><title level="j">The American Journal of Pathology</title>
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<front><div type="abstract" xml:lang="en"><p>Primary lymphedema is a congenital pathology of dysfunctional lymphatic drainage characterized by swelling of the limbs, thickening of the dermis, and fluid and lipid accumulation in the underlying tissue. Two mouse models of primary lymphedema, the Chy mouse and the K14-VEGFR-3-Ig mouse, both lack dermal lymphatic capillaries and exhibit a lymphedematous phenotype attributable to disrupted VEGFR-3 signaling. Here we show that the differences in edematous tissue composition between these two models correlated with drastic differences in hydraulic conductivity. The skin of Chy mice possessed significantly higher levels of collagen and fat, whereas K14-VEGFR-3-Ig mouse skin composition was relatively normal, as compared with their respective wild-type controls. Functionally, this resulted in a greatly increased dermal hydraulic conductivity in K14-VEGFR3-Ig, but not Chy, mice. Our data suggest that lymphedema associated with increased collagen and lipid accumulation counteracts an increased hydraulic conductivity associated with dermal swelling, which in turn further limits interstitial transport and swelling. Without lipid and collagen accumulation, hydraulic conductivity is increased and overall swelling is minimized. These opposing tissue responses to primary lymphedema imply that tissue remodeling—predominantly collagen and fat deposition—may dictate tissue swelling and govern interstitial transport in lymphedema.</p>
</div>
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<author><name sortKey="Rutkowski, Joseph M" sort="Rutkowski, Joseph M" uniqKey="Rutkowski J" first="Joseph M" last="Rutkowski">Joseph M. Rutkowski</name>
<affiliation wicri:level="1"><nlm:affiliation>Institute of Bioengineering, School of Life Sciences/LMBM/Station 15, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland.</nlm:affiliation>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Institute of Bioengineering, School of Life Sciences/LMBM/Station 15, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne</wicri:regionArea>
<placeName><settlement type="city">Lausanne</settlement>
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<author><name sortKey="Markhus, Carl Erik" sort="Markhus, Carl Erik" uniqKey="Markhus C" first="Carl Erik" last="Markhus">Carl Erik Markhus</name>
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<author><name sortKey="Gyenge, Christina C" sort="Gyenge, Christina C" uniqKey="Gyenge C" first="Christina C" last="Gyenge">Christina C. Gyenge</name>
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<author><name sortKey="Alitalo, Kari" sort="Alitalo, Kari" uniqKey="Alitalo K" first="Kari" last="Alitalo">Kari Alitalo</name>
<affiliation><country>Finlande</country>
<placeName><settlement type="city">Helsinki</settlement>
<region type="région" nuts="2">Uusimaa</region>
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<author><name sortKey="Wiig, Helge" sort="Wiig, Helge" uniqKey="Wiig H" first="Helge" last="Wiig">Helge Wiig</name>
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<author><name sortKey="Swartz, Melody A" sort="Swartz, Melody A" uniqKey="Swartz M" first="Melody A" last="Swartz">Melody A. Swartz</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">Dermal collagen and lipid deposition correlate with tissue swelling and hydraulic conductivity in murine primary lymphedema.</title>
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<author><name sortKey="Markhus, Carl Erik" sort="Markhus, Carl Erik" uniqKey="Markhus C" first="Carl Erik" last="Markhus">Carl Erik Markhus</name>
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<author><name sortKey="Gyenge, Christina C" sort="Gyenge, Christina C" uniqKey="Gyenge C" first="Christina C" last="Gyenge">Christina C. Gyenge</name>
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<author><name sortKey="Alitalo, Kari" sort="Alitalo, Kari" uniqKey="Alitalo K" first="Kari" last="Alitalo">Kari Alitalo</name>
<affiliation><country>Finlande</country>
<placeName><settlement type="city">Helsinki</settlement>
<region type="région" nuts="2">Uusimaa</region>
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<term>Biomechanical Phenomena</term>
<term>Collagen (metabolism)</term>
<term>Dermis (metabolism)</term>
<term>Dermis (pathology)</term>
<term>Dermis (physiopathology)</term>
<term>Disease Models, Animal</term>
<term>Extracellular Fluid (metabolism)</term>
<term>Female</term>
<term>Humans</term>
<term>Lipid Metabolism</term>
<term>Lymphedema (metabolism)</term>
<term>Lymphedema (pathology)</term>
<term>Lymphedema (physiopathology)</term>
<term>Male</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Phenotype</term>
<term>Pressure</term>
<term>Vascular Endothelial Growth Factor Receptor-3 (metabolism)</term>
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<term>Collagène (métabolisme)</term>
<term>Derme (anatomopathologie)</term>
<term>Derme (métabolisme)</term>
<term>Derme (physiopathologie)</term>
<term>Femelle</term>
<term>Humains</term>
<term>Liquide extracellulaire (métabolisme)</term>
<term>Lymphoedème (anatomopathologie)</term>
<term>Lymphoedème (métabolisme)</term>
<term>Lymphoedème (physiopathologie)</term>
<term>Modèles animaux de maladie humaine</term>
<term>Mâle</term>
<term>Métabolisme des lipides</term>
<term>Phénomènes biomécaniques</term>
<term>Phénotype</term>
<term>Pression</term>
<term>Récepteur-3 au facteur croissance endothéliale vasculaire (métabolisme)</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
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<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Collagen</term>
<term>Vascular Endothelial Growth Factor Receptor-3</term>
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<term>Liquide extracellulaire</term>
<term>Lymphoedème</term>
<term>Récepteur-3 au facteur croissance endothéliale vasculaire</term>
</keywords>
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<term>Lymphedema</term>
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<term>Biomechanical Phenomena</term>
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<term>Humans</term>
<term>Lipid Metabolism</term>
<term>Male</term>
<term>Mice</term>
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<term>Modèles animaux de maladie humaine</term>
<term>Mâle</term>
<term>Métabolisme des lipides</term>
<term>Phénomènes biomécaniques</term>
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<front><div type="abstract" xml:lang="en">Primary lymphedema is a congenital pathology of dysfunctional lymphatic drainage characterized by swelling of the limbs, thickening of the dermis, and fluid and lipid accumulation in the underlying tissue. Two mouse models of primary lymphedema, the Chy mouse and the K14-VEGFR-3-Ig mouse, both lack dermal lymphatic capillaries and exhibit a lymphedematous phenotype attributable to disrupted VEGFR-3 signaling. Here we show that the differences in edematous tissue composition between these two models correlated with drastic differences in hydraulic conductivity. The skin of Chy mice possessed significantly higher levels of collagen and fat, whereas K14-VEGFR-3-Ig mouse skin composition was relatively normal, as compared with their respective wild-type controls. Functionally, this resulted in a greatly increased dermal hydraulic conductivity in K14-VEGFR3-Ig, but not Chy, mice. Our data suggest that lymphedema associated with increased collagen and lipid accumulation counteracts an increased hydraulic conductivity associated with dermal swelling, which in turn further limits interstitial transport and swelling. Without lipid and collagen accumulation, hydraulic conductivity is increased and overall swelling is minimized. These opposing tissue responses to primary lymphedema imply that tissue remodeling--predominantly collagen and fat deposition--may dictate tissue swelling and govern interstitial transport in lymphedema.</div>
</front>
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