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Pkd1 regulates lymphatic vascular morphogenesis during development

Identifieur interne : 003602 ( Pmc/Corpus ); précédent : 003601; suivant : 003603

Pkd1 regulates lymphatic vascular morphogenesis during development

Auteurs : Baptiste Coxam ; Amélie Sabine ; Neil I. Bower ; Kelly A. Smith ; Cathy Pichol-Thievend ; Renae Skoczylas ; Jonathan W. Astin ; Emmanuelle Frampton ; Muriel Jaquet ; Philip S. Crosier ; Robert G. Parton ; Natasha L. Harvey ; Tatiana V. Petrova ; Stefan Schulte-Merker ; Mathias Francois ; Benjamin M. Hogan

Source :

RBID : PMC:5005109

Abstract

Lymphatic vessels arise during development through sprouting of precursor cells from veins, which is regulated by well-studied signaling and transcriptional mechanisms. Less well understood is the ongoing elaboration of vessels to form a network. This involves cell polarisation, coordinated migration, adhesion, mixing, regression and cell shape rearrangements. We identified a zebrafish mutant, lymphatic and cardiac defects 1 (lyc1), with reduced lymphatic vessel development. We found a mutation in polycystic kidney disease 1a to be responsible for the phenotype. PKD1 is the most frequently mutated gene in autosomal dominant polycystic kidney disease (ADPKD). Initial sprouting of lymphatic precursors is normal in lyc1 mutants, but ongoing migration fails. Loss of Pkd1 in mice also has no effect on sprouting of precursors but leads to failed morphogenesis of the subcutaneous lymphatic network. Individual lymphatic endothelial cells display defective polarity, elongation and adherens junctions. This work identifies a highly selective and unexpected role for Pkd1 in lymphatic vessel morphogenesis during development.


Url:
DOI: 10.1016/j.celrep.2014.03.063
PubMed: 24767999
PubMed Central: 5005109

Links to Exploration step

PMC:5005109

Le document en format XML

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<name sortKey="Schulte Merker, Stefan" sort="Schulte Merker, Stefan" uniqKey="Schulte Merker S" first="Stefan" last="Schulte-Merker">Stefan Schulte-Merker</name>
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<nlm:aff id="A1">Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD 4072, Australia</nlm:aff>
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<name sortKey="Sabine, Amelie" sort="Sabine, Amelie" uniqKey="Sabine A" first="Amélie" last="Sabine">Amélie Sabine</name>
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<nlm:aff id="A2">Department of Oncology, University Hospital of Lausanne, and Department of Biochemistry, University of Lausanne, 1066 Epalinges, Switzerland</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Bower, Neil I" sort="Bower, Neil I" uniqKey="Bower N" first="Neil I." last="Bower">Neil I. Bower</name>
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<name sortKey="Smith, Kelly A" sort="Smith, Kelly A" uniqKey="Smith K" first="Kelly A." last="Smith">Kelly A. Smith</name>
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<nlm:aff id="A1">Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD 4072, Australia</nlm:aff>
</affiliation>
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<name sortKey="Pichol Thievend, Cathy" sort="Pichol Thievend, Cathy" uniqKey="Pichol Thievend C" first="Cathy" last="Pichol-Thievend">Cathy Pichol-Thievend</name>
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<nlm:aff id="A1">Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD 4072, Australia</nlm:aff>
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<name sortKey="Skoczylas, Renae" sort="Skoczylas, Renae" uniqKey="Skoczylas R" first="Renae" last="Skoczylas">Renae Skoczylas</name>
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<nlm:aff id="A1">Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD 4072, Australia</nlm:aff>
</affiliation>
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<name sortKey="Astin, Jonathan W" sort="Astin, Jonathan W" uniqKey="Astin J" first="Jonathan W." last="Astin">Jonathan W. Astin</name>
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<nlm:aff id="A3">Department of Molecular Medicine and Pathology, School of Medical Sciences, The University of Auckland, 1142 Auckland, New Zealand</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Frampton, Emmanuelle" sort="Frampton, Emmanuelle" uniqKey="Frampton E" first="Emmanuelle" last="Frampton">Emmanuelle Frampton</name>
<affiliation>
<nlm:aff id="A1">Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD 4072, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Jaquet, Muriel" sort="Jaquet, Muriel" uniqKey="Jaquet M" first="Muriel" last="Jaquet">Muriel Jaquet</name>
<affiliation>
<nlm:aff id="A2">Department of Oncology, University Hospital of Lausanne, and Department of Biochemistry, University of Lausanne, 1066 Epalinges, Switzerland</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Crosier, Philip S" sort="Crosier, Philip S" uniqKey="Crosier P" first="Philip S." last="Crosier">Philip S. Crosier</name>
<affiliation>
<nlm:aff id="A3">Department of Molecular Medicine and Pathology, School of Medical Sciences, The University of Auckland, 1142 Auckland, New Zealand</nlm:aff>
</affiliation>
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<name sortKey="Parton, Robert G" sort="Parton, Robert G" uniqKey="Parton R" first="Robert G." last="Parton">Robert G. Parton</name>
<affiliation>
<nlm:aff id="A1">Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD 4072, Australia</nlm:aff>
</affiliation>
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<name sortKey="Harvey, Natasha L" sort="Harvey, Natasha L" uniqKey="Harvey N" first="Natasha L." last="Harvey">Natasha L. Harvey</name>
<affiliation>
<nlm:aff id="A4">Division of Haematology, Centre for Cancer Biology, SA Pathology, Adelaide, SA 5000, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Petrova, Tatiana V" sort="Petrova, Tatiana V" uniqKey="Petrova T" first="Tatiana V." last="Petrova">Tatiana V. Petrova</name>
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<nlm:aff id="A2">Department of Oncology, University Hospital of Lausanne, and Department of Biochemistry, University of Lausanne, 1066 Epalinges, Switzerland</nlm:aff>
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<name sortKey="Schulte Merker, Stefan" sort="Schulte Merker, Stefan" uniqKey="Schulte Merker S" first="Stefan" last="Schulte-Merker">Stefan Schulte-Merker</name>
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<nlm:aff id="A5">Hubrecht Institute-KNAW & UMC Utrecht, 3584CT Utrecht, The Netherlands</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Francois, Mathias" sort="Francois, Mathias" uniqKey="Francois M" first="Mathias" last="Francois">Mathias Francois</name>
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<nlm:aff id="A1">Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD 4072, Australia</nlm:aff>
</affiliation>
</author>
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<name sortKey="Hogan, Benjamin M" sort="Hogan, Benjamin M" uniqKey="Hogan B" first="Benjamin M." last="Hogan">Benjamin M. Hogan</name>
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<nlm:aff id="A1">Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD 4072, Australia</nlm:aff>
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<div type="abstract" xml:lang="en">
<p id="P1">Lymphatic vessels arise during development through sprouting of precursor cells from veins, which is regulated by well-studied signaling and transcriptional mechanisms. Less well understood is the ongoing elaboration of vessels to form a network. This involves cell polarisation, coordinated migration, adhesion, mixing, regression and cell shape rearrangements. We identified a zebrafish mutant,
<italic>lymphatic and cardiac defects 1 (lyc1),</italic>
with reduced lymphatic vessel development. We found a mutation in
<italic>polycystic kidney disease 1a</italic>
to be responsible for the phenotype.
<italic>PKD1</italic>
is the most frequently mutated gene in autosomal dominant polycystic kidney disease (ADPKD). Initial sprouting of lymphatic precursors is normal in
<italic>lyc1</italic>
mutants, but ongoing migration fails. Loss of
<italic>Pkd1</italic>
in mice also has no effect on sprouting of precursors but leads to failed morphogenesis of the subcutaneous lymphatic network. Individual lymphatic endothelial cells display defective polarity, elongation and adherens junctions. This work identifies a highly selective and unexpected role for
<italic>Pkd1</italic>
in lymphatic vessel morphogenesis during development.</p>
</div>
</front>
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<journal-id journal-id-type="nlm-journal-id">101573691</journal-id>
<journal-id journal-id-type="pubmed-jr-id">39703</journal-id>
<journal-id journal-id-type="nlm-ta">Cell Rep</journal-id>
<journal-id journal-id-type="iso-abbrev">Cell Rep</journal-id>
<journal-title-group>
<journal-title>Cell reports</journal-title>
</journal-title-group>
<issn pub-type="epub">2211-1247</issn>
</journal-meta>
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<article-id pub-id-type="pmid">24767999</article-id>
<article-id pub-id-type="pmc">5005109</article-id>
<article-id pub-id-type="doi">10.1016/j.celrep.2014.03.063</article-id>
<article-id pub-id-type="manuscript">NIHMS812538</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Pkd1 regulates lymphatic vascular morphogenesis during development</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Coxam</surname>
<given-names>Baptiste</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sabine</surname>
<given-names>Amélie</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Bower</surname>
<given-names>Neil I.</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Smith</surname>
<given-names>Kelly A.</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pichol-Thievend</surname>
<given-names>Cathy</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Skoczylas</surname>
<given-names>Renae</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Astin</surname>
<given-names>Jonathan W.</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Frampton</surname>
<given-names>Emmanuelle</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Jaquet</surname>
<given-names>Muriel</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Crosier</surname>
<given-names>Philip S.</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Parton</surname>
<given-names>Robert G.</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Harvey</surname>
<given-names>Natasha L.</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Petrova</surname>
<given-names>Tatiana V.</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Schulte-Merker</surname>
<given-names>Stefan</given-names>
</name>
<xref ref-type="aff" rid="A5">5</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Francois</surname>
<given-names>Mathias</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref rid="FN2" ref-type="author-notes">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hogan</surname>
<given-names>Benjamin M.</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref rid="FN2" ref-type="author-notes">*</xref>
<xref rid="FN1" ref-type="author-notes">#</xref>
</contrib>
</contrib-group>
<aff id="A1">
<label>1</label>
Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD 4072, Australia</aff>
<aff id="A2">
<label>2</label>
Department of Oncology, University Hospital of Lausanne, and Department of Biochemistry, University of Lausanne, 1066 Epalinges, Switzerland</aff>
<aff id="A3">
<label>3</label>
Department of Molecular Medicine and Pathology, School of Medical Sciences, The University of Auckland, 1142 Auckland, New Zealand</aff>
<aff id="A4">
<label>4</label>
Division of Haematology, Centre for Cancer Biology, SA Pathology, Adelaide, SA 5000, Australia</aff>
<aff id="A5">
<label>5</label>
Hubrecht Institute-KNAW & UMC Utrecht, 3584CT Utrecht, The Netherlands</aff>
<author-notes>
<corresp id="FN1">
<label>#</label>
Corresponding author: Dr Ben Hogan, Division of Molecular Genetics and Development, Institute for Molecular Bioscience, University of Queensland, St Lucia, 4072 QLD, AUSTRALIA,
<email>b.hogan@imb.uq.edu.au</email>
</corresp>
<fn id="FN2">
<label>*</label>
<p>Joint last authors</p>
</fn>
</author-notes>
<pub-date pub-type="nihms-submitted">
<day>25</day>
<month>8</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub">
<day>24</day>
<month>4</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="ppub">
<day>8</day>
<month>5</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>30</day>
<month>8</month>
<year>2016</year>
</pub-date>
<volume>7</volume>
<issue>3</issue>
<fpage>623</fpage>
<lpage>633</lpage>
<pmc-comment>elocation-id from pubmed: 10.1016/j.celrep.2014.03.063</pmc-comment>
<abstract>
<p id="P1">Lymphatic vessels arise during development through sprouting of precursor cells from veins, which is regulated by well-studied signaling and transcriptional mechanisms. Less well understood is the ongoing elaboration of vessels to form a network. This involves cell polarisation, coordinated migration, adhesion, mixing, regression and cell shape rearrangements. We identified a zebrafish mutant,
<italic>lymphatic and cardiac defects 1 (lyc1),</italic>
with reduced lymphatic vessel development. We found a mutation in
<italic>polycystic kidney disease 1a</italic>
to be responsible for the phenotype.
<italic>PKD1</italic>
is the most frequently mutated gene in autosomal dominant polycystic kidney disease (ADPKD). Initial sprouting of lymphatic precursors is normal in
<italic>lyc1</italic>
mutants, but ongoing migration fails. Loss of
<italic>Pkd1</italic>
in mice also has no effect on sprouting of precursors but leads to failed morphogenesis of the subcutaneous lymphatic network. Individual lymphatic endothelial cells display defective polarity, elongation and adherens junctions. This work identifies a highly selective and unexpected role for
<italic>Pkd1</italic>
in lymphatic vessel morphogenesis during development.</p>
</abstract>
</article-meta>
</front>
</pmc>
</record>

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