Ectodomain Shedding of Lymphatic Vessel Endothelial Hyaluronan Receptor 1 (LYVE-1) Is Induced by Vascular Endothelial Growth Factor A (VEGF-A)*
Identifieur interne : 008012 ( Ncbi/Merge ); précédent : 008011; suivant : 008013Ectodomain Shedding of Lymphatic Vessel Endothelial Hyaluronan Receptor 1 (LYVE-1) Is Induced by Vascular Endothelial Growth Factor A (VEGF-A)*
Auteurs : Hisayo Nishida-Fukuda ; Ryoichi Araki ; Masachika Shudou [Japon] ; Hidenori Okazaki ; Yasuko Tomono [Japon] ; Hironao Nakayama [Japon] ; Shinji Fukuda [Japon] ; Tomohisa Sakaue [Japon] ; Yuji Shirakata ; Koji Sayama ; Koji Hashimoto ; Michael Detmar [Suisse] ; Shigeki Higashiyama [Japon] ; Satoshi Hirakawa [Japon]Source :
- The Journal of Biological Chemistry [ 0021-9258 ] ; 2016.
Abstract
Lymphatic vessel endothelial hyaluronan receptor 1 (LYVE-1), a type I transmembrane glycoprotein, is known as one of the most specific lymphatic vessel markers in the skin. In this study, we found that the ectodomain of LYVE-1 undergoes proteolytic cleavage, and this process produces soluble LYVE-1. We further identified the cleavage site for ectodomain shedding and generated an uncleavable mutant of LYVE-1. In lymphatic endothelial cells, ectodomain shedding of LYVE-1 was induced by vascular endothelial growth factor (VEGF)-A, an important factor for angiogenesis and lymphangiogenesis under pathological conditions. VEGF-A-induced LYVE-1 ectodomain shedding was mediated via the extracellular signal-regulated kinase (ERK) and a disintegrin and metalloproteinase (ADAM) 17. Wild-type LYVE-1, but not uncleavable LYVE-1, promoted migration of lymphatic endothelial cells in response to VEGF-A. Immunostaining analyses in human psoriasis skin lesions and VEGF-A transgenic mouse skin suggested that the ectodomain shedding of LYVE-1 occurred in lymphatic vessels undergoing chronic inflammation. These results indicate that the ectodomain shedding of LYVE-1 might be involved in promoting pathological lymphangiogenesis.
Url:
DOI: 10.1074/jbc.M115.683201
PubMed: 26966180
PubMed Central: 4865900
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<front><div type="abstract" xml:lang="en"><p>Lymphatic vessel endothelial hyaluronan receptor 1 (LYVE-1), a type I transmembrane glycoprotein, is known as one of the most specific lymphatic vessel markers in the skin. In this study, we found that the ectodomain of LYVE-1 undergoes proteolytic cleavage, and this process produces soluble LYVE-1. We further identified the cleavage site for ectodomain shedding and generated an uncleavable mutant of LYVE-1. In lymphatic endothelial cells, ectodomain shedding of LYVE-1 was induced by vascular endothelial growth factor (VEGF)-A, an important factor for angiogenesis and lymphangiogenesis under pathological conditions. VEGF-A-induced LYVE-1 ectodomain shedding was mediated via the extracellular signal-regulated kinase (ERK) and a disintegrin and metalloproteinase (ADAM) 17. Wild-type LYVE-1, but not uncleavable LYVE-1, promoted migration of lymphatic endothelial cells in response to VEGF-A. Immunostaining analyses in human psoriasis skin lesions and VEGF-A transgenic mouse skin suggested that the ectodomain shedding of LYVE-1 occurred in lymphatic vessels undergoing chronic inflammation. These results indicate that the ectodomain shedding of LYVE-1 might be involved in promoting pathological lymphangiogenesis.</p>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">J Biol Chem</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Biol. Chem</journal-id>
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</subj-group>
</article-categories>
<title-group><article-title>Ectodomain Shedding of Lymphatic Vessel Endothelial Hyaluronan Receptor 1 (LYVE-1) Is Induced by Vascular Endothelial Growth Factor A (VEGF-A)<xref ref-type="fn" rid="FN1">*</xref>
</article-title>
<alt-title alt-title-type="short">VEGF-induced LYVE-1 Shedding in Lymphatic Endothelial Cells</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Nishida-Fukuda</surname>
<given-names>Hisayo</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Araki</surname>
<given-names>Ryoichi</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Shudou</surname>
<given-names>Masachika</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>¶</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Okazaki</surname>
<given-names>Hidenori</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Tomono</surname>
<given-names>Yasuko</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>‖</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Nakayama</surname>
<given-names>Hironao</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
<xref ref-type="aff" rid="aff5">**</xref>
<xref ref-type="aff" rid="aff6"><sup>‡‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fukuda</surname>
<given-names>Shinji</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>‡‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sakaue</surname>
<given-names>Tomohisa</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>‡‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Shirakata</surname>
<given-names>Yuji</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sayama</surname>
<given-names>Koji</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hashimoto</surname>
<given-names>Koji</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Detmar</surname>
<given-names>Michael</given-names>
</name>
<xref ref-type="aff" rid="aff7"><sup>§§</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Higashiyama</surname>
<given-names>Shigeki</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
<xref ref-type="aff" rid="aff5">**</xref>
<xref ref-type="aff" rid="aff6"><sup>‡‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hirakawa</surname>
<given-names>Satoshi</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff5">**</xref>
<xref ref-type="aff" rid="aff8"><sup>¶¶</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>1</sup>
</xref>
</contrib>
<aff id="aff1">From the Departments of<label>‡</label>
Dermatology,</aff>
<aff id="aff2"><label>§</label>
Biochemistry and Molecular Genetics, and</aff>
<aff id="aff3"><label>¶</label>
Bioscience, Advanced Research Support Center (ADRES), Ehime University Graduate School of Medicine, Toon 791-0295, Japan,</aff>
<aff id="aff4"><label>‖</label>
Division of Molecular and Cell Biology, Shigei Medical Research Institute, Okayama 701-0202, Japan,</aff>
<aff id="aff5"><label>**</label>
Strategic Young Researcher Overseas Visiting Program for Accelerating Brain Circulation, Japan Society for the Promotion of Science (JSPS), 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan,</aff>
<aff id="aff6"><label>‡‡</label>
Division of Cell Growth and Tumor Regulation, Proteo-Science Center (PROS), Ehime University, Toon 791-0295, Japan,</aff>
<aff id="aff7"><label>§§</label>
Institute of Pharmaceutical Sciences, Swiss Federal Institute of Technology, ETH Zurich, Zurich CH-8093, Switzerland, and</aff>
<aff id="aff8"><label>¶¶</label>
Department of Dermatology, Hamamatsu University School of Medicine, Hamamatsu 431-3192, Japan</aff>
</contrib-group>
<author-notes><corresp id="cor1"><label>1</label>
To whom correspondence should be addressed: <addr-line>Dept. of Dermatology, Hamamatsu University School of Medicine, Handayama 1-20-1, Higashi-ku, Hamamatsu 431-3192, Japan.</addr-line>
Tel.: <phone>81-53-435-2065</phone>
; Fax: <fax>81-53-435-2368</fax>
; E-mail: <email>hirakawa@hama-med.ac.jp</email>
.</corresp>
</author-notes>
<pub-date pub-type="ppub"><day>13</day>
<month>5</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub"><day>10</day>
<month>3</month>
<year>2016</year>
</pub-date>
<volume>291</volume>
<issue>20</issue>
<fpage>10490</fpage>
<lpage>10500</lpage>
<history><date date-type="received"><day>3</day>
<month>8</month>
<year>2015</year>
</date>
<date date-type="rev-recd"><day>7</day>
<month>3</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>© 2016 by The American Society for Biochemistry and Molecular Biology, Inc.</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>The American Society for Biochemistry and Molecular Biology, Inc.</copyright-holder>
</permissions>
<self-uri content-type="pdf" xlink:href="zbc02016010490.pdf"></self-uri>
<abstract><p>Lymphatic vessel endothelial hyaluronan receptor 1 (LYVE-1), a type I transmembrane glycoprotein, is known as one of the most specific lymphatic vessel markers in the skin. In this study, we found that the ectodomain of LYVE-1 undergoes proteolytic cleavage, and this process produces soluble LYVE-1. We further identified the cleavage site for ectodomain shedding and generated an uncleavable mutant of LYVE-1. In lymphatic endothelial cells, ectodomain shedding of LYVE-1 was induced by vascular endothelial growth factor (VEGF)-A, an important factor for angiogenesis and lymphangiogenesis under pathological conditions. VEGF-A-induced LYVE-1 ectodomain shedding was mediated via the extracellular signal-regulated kinase (ERK) and a disintegrin and metalloproteinase (ADAM) 17. Wild-type LYVE-1, but not uncleavable LYVE-1, promoted migration of lymphatic endothelial cells in response to VEGF-A. Immunostaining analyses in human psoriasis skin lesions and VEGF-A transgenic mouse skin suggested that the ectodomain shedding of LYVE-1 occurred in lymphatic vessels undergoing chronic inflammation. These results indicate that the ectodomain shedding of LYVE-1 might be involved in promoting pathological lymphangiogenesis.</p>
</abstract>
<kwd-group><kwd>ADAM</kwd>
<kwd>endothelial cell</kwd>
<kwd>extracellular signal-regulated kinase (ERK)</kwd>
<kwd>hyaluronan</kwd>
<kwd>lymphangiogenesis</kwd>
<kwd>psoriasis</kwd>
<kwd>shedding</kwd>
<kwd>skin</kwd>
<kwd>vascular endothelial growth factor (VEGF)</kwd>
<kwd>lymphatic endothelial hyaluronan receptor 1 (LYVE-1)</kwd>
</kwd-group>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Japon</li>
<li>Suisse</li>
</country>
<region><li>Région de Kantō</li>
</region>
<settlement><li>Tokyo</li>
</settlement>
</list>
<tree><noCountry><name sortKey="Araki, Ryoichi" sort="Araki, Ryoichi" uniqKey="Araki R" first="Ryoichi" last="Araki">Ryoichi Araki</name>
<name sortKey="Hashimoto, Koji" sort="Hashimoto, Koji" uniqKey="Hashimoto K" first="Koji" last="Hashimoto">Koji Hashimoto</name>
<name sortKey="Nishida Fukuda, Hisayo" sort="Nishida Fukuda, Hisayo" uniqKey="Nishida Fukuda H" first="Hisayo" last="Nishida-Fukuda">Hisayo Nishida-Fukuda</name>
<name sortKey="Okazaki, Hidenori" sort="Okazaki, Hidenori" uniqKey="Okazaki H" first="Hidenori" last="Okazaki">Hidenori Okazaki</name>
<name sortKey="Sayama, Koji" sort="Sayama, Koji" uniqKey="Sayama K" first="Koji" last="Sayama">Koji Sayama</name>
<name sortKey="Shirakata, Yuji" sort="Shirakata, Yuji" uniqKey="Shirakata Y" first="Yuji" last="Shirakata">Yuji Shirakata</name>
</noCountry>
<country name="Japon"><noRegion><name sortKey="Shudou, Masachika" sort="Shudou, Masachika" uniqKey="Shudou M" first="Masachika" last="Shudou">Masachika Shudou</name>
</noRegion>
<name sortKey="Fukuda, Shinji" sort="Fukuda, Shinji" uniqKey="Fukuda S" first="Shinji" last="Fukuda">Shinji Fukuda</name>
<name sortKey="Higashiyama, Shigeki" sort="Higashiyama, Shigeki" uniqKey="Higashiyama S" first="Shigeki" last="Higashiyama">Shigeki Higashiyama</name>
<name sortKey="Higashiyama, Shigeki" sort="Higashiyama, Shigeki" uniqKey="Higashiyama S" first="Shigeki" last="Higashiyama">Shigeki Higashiyama</name>
<name sortKey="Hirakawa, Satoshi" sort="Hirakawa, Satoshi" uniqKey="Hirakawa S" first="Satoshi" last="Hirakawa">Satoshi Hirakawa</name>
<name sortKey="Hirakawa, Satoshi" sort="Hirakawa, Satoshi" uniqKey="Hirakawa S" first="Satoshi" last="Hirakawa">Satoshi Hirakawa</name>
<name sortKey="Nakayama, Hironao" sort="Nakayama, Hironao" uniqKey="Nakayama H" first="Hironao" last="Nakayama">Hironao Nakayama</name>
<name sortKey="Nakayama, Hironao" sort="Nakayama, Hironao" uniqKey="Nakayama H" first="Hironao" last="Nakayama">Hironao Nakayama</name>
<name sortKey="Sakaue, Tomohisa" sort="Sakaue, Tomohisa" uniqKey="Sakaue T" first="Tomohisa" last="Sakaue">Tomohisa Sakaue</name>
<name sortKey="Tomono, Yasuko" sort="Tomono, Yasuko" uniqKey="Tomono Y" first="Yasuko" last="Tomono">Yasuko Tomono</name>
</country>
<country name="Suisse"><noRegion><name sortKey="Detmar, Michael" sort="Detmar, Michael" uniqKey="Detmar M" first="Michael" last="Detmar">Michael Detmar</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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