Laminar flow downregulates Notch activity to promote lymphatic sprouting
Identifieur interne : 012C63 ( Main/Exploration ); précédent : 012C62; suivant : 012C64Laminar flow downregulates Notch activity to promote lymphatic sprouting
Auteurs : Dongwon Choi [États-Unis] ; Eunkyung Park [États-Unis] ; Eunson Jung [États-Unis] ; Young Jin Seong [États-Unis] ; Jaehyuk Yoo [États-Unis] ; Esak Lee [États-Unis] ; Mingu Hong [États-Unis] ; Sunju Lee [États-Unis] ; Hiroaki Ishida [Canada] ; James Burford [États-Unis] ; Janos Peti-Peterdi [États-Unis] ; Ralf H. Adams [Allemagne] ; Sonal Srikanth [États-Unis] ; Yousang Gwack [États-Unis] ; Christopher S. Chen [États-Unis] ; Hans J. Vogel [Canada] ; Chester J. Koh [États-Unis] ; Alex K. Wong [États-Unis] ; Young-Kwon Hong [États-Unis]Source :
- The Journal of Clinical Investigation [ 0021-9738 ] ; ????.
Abstract
The major function of the lymphatic system is to drain interstitial fluid from tissue. Functional drainage causes increased fluid flow that triggers lymphatic expansion, which is conceptually similar to hypoxia-triggered angiogenesis. Here, we have identified a mechanotransduction pathway that translates laminar flow–induced shear stress to activation of lymphatic sprouting. While low-rate laminar flow commonly induces the classic shear stress responses in blood endothelial cells and lymphatic endothelial cells (LECs), only LECs display reduced Notch activity and increased sprouting capacity. In response to flow, the plasma membrane calcium channel ORAI1 mediates calcium influx in LECs and activates calmodulin to facilitate a physical interaction between Krüppel-like factor 2 (KLF2), the major regulator of shear responses, and PROX1, the master regulator of lymphatic development. The PROX1/KLF2 complex upregulates the expression of
Url:
DOI: 10.1172/JCI87442
PubMed: 28263185
PubMed Central: 5373895
Affiliations:
- Allemagne, Canada, États-Unis
- Alberta, Californie, District de Münster, Massachusetts, Rhénanie-du-Nord-Westphalie, Texas
- Calgary, Los Angeles, Münster
- Université de Calgary, Université de Californie du Sud
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Le document en format XML
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<affiliation wicri:level="4"><nlm:aff id="A3">Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada.</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">Canada</country>
<wicri:regionArea>Department of Biological Sciences, University of Calgary, Calgary, Alberta</wicri:regionArea>
<orgName type="university">Université de Calgary</orgName>
<placeName><settlement type="city">Calgary</settlement>
<region type="state">Alberta</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Burford, James" sort="Burford, James" uniqKey="Burford J" first="James" last="Burford">James Burford</name>
<affiliation wicri:level="4"><nlm:aff id="A4">Department of Physiology and Biophysics, Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">États-Unis</country>
<wicri:regionArea>Department of Physiology and Biophysics, Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Los Angeles, California</wicri:regionArea>
<placeName><region type="state">Californie</region>
<settlement type="city">Los Angeles</settlement>
</placeName>
<orgName type="university">Université de Californie du Sud</orgName>
</affiliation>
</author>
<author><name sortKey="Peti Peterdi, Janos" sort="Peti Peterdi, Janos" uniqKey="Peti Peterdi J" first="Janos" last="Peti-Peterdi">Janos Peti-Peterdi</name>
<affiliation wicri:level="4"><nlm:aff id="A4">Department of Physiology and Biophysics, Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">États-Unis</country>
<wicri:regionArea>Department of Physiology and Biophysics, Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Los Angeles, California</wicri:regionArea>
<placeName><region type="state">Californie</region>
<settlement type="city">Los Angeles</settlement>
</placeName>
<orgName type="university">Université de Californie du Sud</orgName>
</affiliation>
</author>
<author><name sortKey="Adams, Ralf H" sort="Adams, Ralf H" uniqKey="Adams R" first="Ralf H." last="Adams">Ralf H. Adams</name>
<affiliation wicri:level="3"><nlm:aff id="A5">Max Planck Institute for Molecular Biomedicine, Department of Tissue Morphogenesis, and University of Münster, Faculty of Medicine, Münster, Germany.</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">Allemagne</country>
<wicri:regionArea>Max Planck Institute for Molecular Biomedicine, Department of Tissue Morphogenesis, and University of Münster, Faculty of Medicine, Münster</wicri:regionArea>
<placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region>
<region type="district" nuts="2">District de Münster</region>
<settlement type="city">Münster</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="Srikanth, Sonal" sort="Srikanth, Sonal" uniqKey="Srikanth S" first="Sonal" last="Srikanth">Sonal Srikanth</name>
<affiliation wicri:level="2"><nlm:aff id="A6">Department of Physiology, David Geffen School of Medicine at UCLA, Los Angeles, California, USA.</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">États-Unis</country>
<wicri:regionArea>Department of Physiology, David Geffen School of Medicine at UCLA, Los Angeles, California</wicri:regionArea>
<placeName><region type="state">Californie</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Gwack, Yousang" sort="Gwack, Yousang" uniqKey="Gwack Y" first="Yousang" last="Gwack">Yousang Gwack</name>
<affiliation wicri:level="2"><nlm:aff id="A6">Department of Physiology, David Geffen School of Medicine at UCLA, Los Angeles, California, USA.</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">États-Unis</country>
<wicri:regionArea>Department of Physiology, David Geffen School of Medicine at UCLA, Los Angeles, California</wicri:regionArea>
<placeName><region type="state">Californie</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Chen, Christopher S" sort="Chen, Christopher S" uniqKey="Chen C" first="Christopher S." last="Chen">Christopher S. Chen</name>
<affiliation wicri:level="2"><nlm:aff id="A2">Department of Biomedical Engineering and the Biological Design Center, Boston University; and Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, Massachusetts, USA.</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">États-Unis</country>
<wicri:regionArea>Department of Biomedical Engineering and the Biological Design Center, Boston University; and Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, Massachusetts</wicri:regionArea>
<placeName><region type="state">Massachusetts</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Vogel, Hans J" sort="Vogel, Hans J" uniqKey="Vogel H" first="Hans J." last="Vogel">Hans J. Vogel</name>
<affiliation wicri:level="4"><nlm:aff id="A3">Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada.</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">Canada</country>
<wicri:regionArea>Department of Biological Sciences, University of Calgary, Calgary, Alberta</wicri:regionArea>
<orgName type="university">Université de Calgary</orgName>
<placeName><settlement type="city">Calgary</settlement>
<region type="state">Alberta</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Koh, Chester J" sort="Koh, Chester J" uniqKey="Koh C" first="Chester J." last="Koh">Chester J. Koh</name>
<affiliation wicri:level="2"><nlm:aff id="A7">Division of Pediatric Urology, Texas Children’s Hospital, Baylor College of Medicine, Houston, Texas, USA.</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">États-Unis</country>
<wicri:regionArea>Division of Pediatric Urology, Texas Children’s Hospital, Baylor College of Medicine, Houston, Texas</wicri:regionArea>
<placeName><region type="state">Texas</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Wong, Alex K" sort="Wong, Alex K" uniqKey="Wong A" first="Alex K." last="Wong">Alex K. Wong</name>
<affiliation wicri:level="4"><nlm:aff id="A1">Division of Plastic and Reconstructive Surgery, Department of Surgery, Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">États-Unis</country>
<wicri:regionArea>Division of Plastic and Reconstructive Surgery, Department of Surgery, Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California</wicri:regionArea>
<placeName><region type="state">Californie</region>
<settlement type="city">Los Angeles</settlement>
</placeName>
<orgName type="university">Université de Californie du Sud</orgName>
</affiliation>
</author>
<author><name sortKey="Hong, Young Kwon" sort="Hong, Young Kwon" uniqKey="Hong Y" first="Young-Kwon" last="Hong">Young-Kwon Hong</name>
<affiliation wicri:level="4"><nlm:aff id="A1">Division of Plastic and Reconstructive Surgery, Department of Surgery, Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.</nlm:aff>
<country xml:lang="fr" wicri:curation="lc">États-Unis</country>
<wicri:regionArea>Division of Plastic and Reconstructive Surgery, Department of Surgery, Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California</wicri:regionArea>
<placeName><region type="state">Californie</region>
<settlement type="city">Los Angeles</settlement>
</placeName>
<orgName type="university">Université de Californie du Sud</orgName>
</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 major function of the lymphatic system is to drain interstitial fluid from tissue. Functional drainage causes increased fluid flow that triggers lymphatic expansion, which is conceptually similar to hypoxia-triggered angiogenesis. Here, we have identified a mechanotransduction pathway that translates laminar flow–induced shear stress to activation of lymphatic sprouting. While low-rate laminar flow commonly induces the classic shear stress responses in blood endothelial cells and lymphatic endothelial cells (LECs), only LECs display reduced Notch activity and increased sprouting capacity. In response to flow, the plasma membrane calcium channel ORAI1 mediates calcium influx in LECs and activates calmodulin to facilitate a physical interaction between Krüppel-like factor 2 (KLF2), the major regulator of shear responses, and PROX1, the master regulator of lymphatic development. The PROX1/KLF2 complex upregulates the expression of <italic>DTX1</italic>
and <italic>DTX3L</italic>
. DTX1 and DTX3L, functioning as a heterodimeric Notch E3 ligase, concertedly downregulate NOTCH1 activity and enhance lymphatic sprouting. Notably, overexpression of the calcium reporter GCaMP3 unexpectedly inhibited lymphatic sprouting, presumably by disturbing calcium signaling. Endothelial-specific knockouts of <italic>Orai1</italic>
and <italic>Klf2</italic>
also markedly impaired lymphatic sprouting. Moreover, <italic>Dtx3l</italic>
loss of function led to defective lymphatic sprouting, while <italic>Dtx3l</italic>
gain of function rescued impaired sprouting in <italic>Orai1</italic>
KO embryos. Together, the data reveal a molecular mechanism underlying laminar flow–induced lymphatic sprouting.</p>
</div>
</front>
</TEI>
<affiliations><list><country><li>Allemagne</li>
<li>Canada</li>
<li>États-Unis</li>
</country>
<region><li>Alberta</li>
<li>Californie</li>
<li>District de Münster</li>
<li>Massachusetts</li>
<li>Rhénanie-du-Nord-Westphalie</li>
<li>Texas</li>
</region>
<settlement><li>Calgary</li>
<li>Los Angeles</li>
<li>Münster</li>
</settlement>
<orgName><li>Université de Calgary</li>
<li>Université de Californie du Sud</li>
</orgName>
</list>
<tree><country name="États-Unis"><region name="Californie"><name sortKey="Choi, Dongwon" sort="Choi, Dongwon" uniqKey="Choi D" first="Dongwon" last="Choi">Dongwon Choi</name>
</region>
<name sortKey="Burford, James" sort="Burford, James" uniqKey="Burford J" first="James" last="Burford">James Burford</name>
<name sortKey="Chen, Christopher S" sort="Chen, Christopher S" uniqKey="Chen C" first="Christopher S." last="Chen">Christopher S. Chen</name>
<name sortKey="Gwack, Yousang" sort="Gwack, Yousang" uniqKey="Gwack Y" first="Yousang" last="Gwack">Yousang Gwack</name>
<name sortKey="Hong, Mingu" sort="Hong, Mingu" uniqKey="Hong M" first="Mingu" last="Hong">Mingu Hong</name>
<name sortKey="Hong, Young Kwon" sort="Hong, Young Kwon" uniqKey="Hong Y" first="Young-Kwon" last="Hong">Young-Kwon Hong</name>
<name sortKey="Jung, Eunson" sort="Jung, Eunson" uniqKey="Jung E" first="Eunson" last="Jung">Eunson Jung</name>
<name sortKey="Koh, Chester J" sort="Koh, Chester J" uniqKey="Koh C" first="Chester J." last="Koh">Chester J. Koh</name>
<name sortKey="Lee, Esak" sort="Lee, Esak" uniqKey="Lee E" first="Esak" last="Lee">Esak Lee</name>
<name sortKey="Lee, Sunju" sort="Lee, Sunju" uniqKey="Lee S" first="Sunju" last="Lee">Sunju Lee</name>
<name sortKey="Park, Eunkyung" sort="Park, Eunkyung" uniqKey="Park E" first="Eunkyung" last="Park">Eunkyung Park</name>
<name sortKey="Peti Peterdi, Janos" sort="Peti Peterdi, Janos" uniqKey="Peti Peterdi J" first="Janos" last="Peti-Peterdi">Janos Peti-Peterdi</name>
<name sortKey="Seong, Young Jin" sort="Seong, Young Jin" uniqKey="Seong Y" first="Young Jin" last="Seong">Young Jin Seong</name>
<name sortKey="Srikanth, Sonal" sort="Srikanth, Sonal" uniqKey="Srikanth S" first="Sonal" last="Srikanth">Sonal Srikanth</name>
<name sortKey="Wong, Alex K" sort="Wong, Alex K" uniqKey="Wong A" first="Alex K." last="Wong">Alex K. Wong</name>
<name sortKey="Yoo, Jaehyuk" sort="Yoo, Jaehyuk" uniqKey="Yoo J" first="Jaehyuk" last="Yoo">Jaehyuk Yoo</name>
</country>
<country name="Canada"><region name="Alberta"><name sortKey="Ishida, Hiroaki" sort="Ishida, Hiroaki" uniqKey="Ishida H" first="Hiroaki" last="Ishida">Hiroaki Ishida</name>
</region>
<name sortKey="Vogel, Hans J" sort="Vogel, Hans J" uniqKey="Vogel H" first="Hans J." last="Vogel">Hans J. Vogel</name>
</country>
<country name="Allemagne"><region name="Rhénanie-du-Nord-Westphalie"><name sortKey="Adams, Ralf H" sort="Adams, Ralf H" uniqKey="Adams R" first="Ralf H." last="Adams">Ralf H. Adams</name>
</region>
</country>
</tree>
</affiliations>
</record>
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