Efficient activation of the lymphangiogenic growth factor VEGF-C requires the C-terminal domain of VEGF-C and the N-terminal domain of CCBE1.
Identifieur interne : 000365 ( PubMed/Checkpoint ); précédent : 000364; suivant : 000366Efficient activation of the lymphangiogenic growth factor VEGF-C requires the C-terminal domain of VEGF-C and the N-terminal domain of CCBE1.
Auteurs : Sawan Kumar Jha [Finlande] ; Khushbu Rauniyar [Finlande] ; Terhi Karpanen [Norvège] ; Veli-Matti Lepp Nen [Finlande] ; Pascal Brouillard [Belgique] ; Miikka Vikkula [Belgique] ; Kari Alitalo [Finlande] ; Michael Jeltsch [Finlande]Source :
- Scientific reports [ 2045-2322 ] ; 2017.
Abstract
The collagen- and calcium-binding EGF domains 1 (CCBE1) protein is necessary for lymphangiogenesis. Its C-terminal collagen-like domain was shown to be required for the activation of the major lymphangiogenic growth factor VEGF-C (Vascular Endothelial Growth Factor-C) along with the ADAMTS3 (A Disintegrin And Metalloproteinase with Thrombospondin Motifs-3) protease. However, it remained unclear how the N-terminal domain of CCBE1 contributed to lymphangiogenic signaling. Here, we show that efficient activation of VEGF-C requires its C-terminal domain both in vitro and in a transgenic mouse model. The N-terminal EGF-like domain of CCBE1 increased VEGFR-3 signaling by colocalizing pro-VEGF-C with its activating protease to the lymphatic endothelial cell surface. When the ADAMTS3 amounts were limited, proteolytic activation of pro-VEGF-C was supported by the N-terminal domain of CCBE1, but not by its C-terminal domain. A single amino acid substitution in ADAMTS3, identified from a lymphedema patient, was associated with abnormal CCBE1 localization. These results show that CCBE1 promotes VEGFR-3 signaling and lymphangiogenesis by different mechanisms, which are mediated independently by the two domains of CCBE1: by enhancing the cleavage activity of ADAMTS3 and by facilitating the colocalization of VEGF-C and ADAMTS3. These new insights should be valuable in developing new strategies to therapeutically target VEGF-C/VEGFR-3-induced lymphangiogenesis.
DOI: 10.1038/s41598-017-04982-1
PubMed: 28687807
Affiliations:
- Belgique, Finlande, Norvège
- Région de Bruxelles-Capitale, Uusimaa, Østlandet
- Bruxelles, Helsinki, Oslo
- Université d'Helsinki
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Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014, Finland.</nlm:affiliation><country xml:lang="fr">Finlande</country><wicri:regionArea>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014</wicri:regionArea><orgName type="university">Université d'Helsinki</orgName><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName></affiliation></author><author><name sortKey="Rauniyar, Khushbu" sort="Rauniyar, Khushbu" uniqKey="Rauniyar K" first="Khushbu" last="Rauniyar">Khushbu Rauniyar</name><affiliation wicri:level="4"><nlm:affiliation>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014, Finland.</nlm:affiliation><country xml:lang="fr">Finlande</country><wicri:regionArea>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014</wicri:regionArea><orgName type="university">Université d'Helsinki</orgName><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName></affiliation></author><author><name sortKey="Karpanen, Terhi" sort="Karpanen, Terhi" uniqKey="Karpanen T" first="Terhi" last="Karpanen">Terhi Karpanen</name><affiliation wicri:level="3"><nlm:affiliation>University Hospital Radiumhospitalet and K. G. Jebsen Center for Cancer Immunotherapy, Institute for Clinical Medicine, University of Oslo, Oslo, Norway.</nlm:affiliation><country xml:lang="fr">Norvège</country><wicri:regionArea>University Hospital Radiumhospitalet and K. G. Jebsen Center for Cancer Immunotherapy, Institute for Clinical Medicine, University of Oslo, Oslo</wicri:regionArea><placeName><settlement type="city">Oslo</settlement><region nuts="2">Østlandet</region></placeName></affiliation></author><author><name sortKey="Lepp Nen, Veli Matti" sort="Lepp Nen, Veli Matti" uniqKey="Lepp Nen V" first="Veli-Matti" last="Lepp Nen">Veli-Matti Lepp Nen</name><affiliation wicri:level="4"><nlm:affiliation>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014, Finland.</nlm:affiliation><country xml:lang="fr">Finlande</country><wicri:regionArea>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014</wicri:regionArea><orgName type="university">Université d'Helsinki</orgName><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName></affiliation></author><author><name sortKey="Brouillard, Pascal" sort="Brouillard, Pascal" uniqKey="Brouillard P" first="Pascal" last="Brouillard">Pascal Brouillard</name><affiliation wicri:level="3"><nlm:affiliation>de Duve Institute, University of Louvain, Brussels, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>de Duve Institute, University of Louvain, Brussels</wicri:regionArea><placeName><settlement type="city">Bruxelles</settlement><region nuts="2">Région de Bruxelles-Capitale</region></placeName></affiliation></author><author><name sortKey="Vikkula, Miikka" sort="Vikkula, Miikka" uniqKey="Vikkula M" first="Miikka" last="Vikkula">Miikka Vikkula</name><affiliation wicri:level="3"><nlm:affiliation>de Duve Institute, University of Louvain, Brussels, Belgium.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>de Duve Institute, University of Louvain, Brussels</wicri:regionArea><placeName><settlement type="city">Bruxelles</settlement><region nuts="2">Région de Bruxelles-Capitale</region></placeName></affiliation></author><author><name sortKey="Alitalo, Kari" sort="Alitalo, Kari" uniqKey="Alitalo K" first="Kari" last="Alitalo">Kari Alitalo</name><affiliation wicri:level="4"><nlm:affiliation>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014, Finland.</nlm:affiliation><country xml:lang="fr">Finlande</country><wicri:regionArea>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014</wicri:regionArea><orgName type="university">Université d'Helsinki</orgName><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName><orgName type="university">Université d'Helsinki</orgName></affiliation></author><author><name sortKey="Jeltsch, Michael" sort="Jeltsch, Michael" uniqKey="Jeltsch M" first="Michael" last="Jeltsch">Michael Jeltsch</name><affiliation wicri:level="4"><nlm:affiliation>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014, Finland. michael@jeltsch.org.</nlm:affiliation><country xml:lang="fr">Finlande</country><wicri:regionArea>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014</wicri:regionArea><orgName type="university">Université d'Helsinki</orgName><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName></affiliation></author></analytic><series><title level="j">Scientific reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The collagen- and calcium-binding EGF domains 1 (CCBE1) protein is necessary for lymphangiogenesis. Its C-terminal collagen-like domain was shown to be required for the activation of the major lymphangiogenic growth factor VEGF-C (Vascular Endothelial Growth Factor-C) along with the ADAMTS3 (A Disintegrin And Metalloproteinase with Thrombospondin Motifs-3) protease. However, it remained unclear how the N-terminal domain of CCBE1 contributed to lymphangiogenic signaling. Here, we show that efficient activation of VEGF-C requires its C-terminal domain both in vitro and in a transgenic mouse model. The N-terminal EGF-like domain of CCBE1 increased VEGFR-3 signaling by colocalizing pro-VEGF-C with its activating protease to the lymphatic endothelial cell surface. When the ADAMTS3 amounts were limited, proteolytic activation of pro-VEGF-C was supported by the N-terminal domain of CCBE1, but not by its C-terminal domain. A single amino acid substitution in ADAMTS3, identified from a lymphedema patient, was associated with abnormal CCBE1 localization. These results show that CCBE1 promotes VEGFR-3 signaling and lymphangiogenesis by different mechanisms, which are mediated independently by the two domains of CCBE1: by enhancing the cleavage activity of ADAMTS3 and by facilitating the colocalization of VEGF-C and ADAMTS3. These new insights should be valuable in developing new strategies to therapeutically target VEGF-C/VEGFR-3-induced lymphangiogenesis.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">28687807</PMID><DateCreated><Year>2017</Year><Month>07</Month><Day>08</Day></DateCreated><DateRevised><Year>2017</Year><Month>09</Month><Day>02</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2045-2322</ISSN><JournalIssue CitedMedium="Internet"><Volume>7</Volume><Issue>1</Issue><PubDate><Year>2017</Year><Month>Jul</Month><Day>07</Day></PubDate></JournalIssue><Title>Scientific reports</Title><ISOAbbreviation>Sci Rep</ISOAbbreviation></Journal><ArticleTitle>Efficient activation of the lymphangiogenic growth factor VEGF-C requires the C-terminal domain of VEGF-C and the N-terminal domain of CCBE1.</ArticleTitle><Pagination><MedlinePgn>4916</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41598-017-04982-1</ELocationID><Abstract><AbstractText>The collagen- and calcium-binding EGF domains 1 (CCBE1) protein is necessary for lymphangiogenesis. Its C-terminal collagen-like domain was shown to be required for the activation of the major lymphangiogenic growth factor VEGF-C (Vascular Endothelial Growth Factor-C) along with the ADAMTS3 (A Disintegrin And Metalloproteinase with Thrombospondin Motifs-3) protease. However, it remained unclear how the N-terminal domain of CCBE1 contributed to lymphangiogenic signaling. Here, we show that efficient activation of VEGF-C requires its C-terminal domain both in vitro and in a transgenic mouse model. The N-terminal EGF-like domain of CCBE1 increased VEGFR-3 signaling by colocalizing pro-VEGF-C with its activating protease to the lymphatic endothelial cell surface. When the ADAMTS3 amounts were limited, proteolytic activation of pro-VEGF-C was supported by the N-terminal domain of CCBE1, but not by its C-terminal domain. A single amino acid substitution in ADAMTS3, identified from a lymphedema patient, was associated with abnormal CCBE1 localization. These results show that CCBE1 promotes VEGFR-3 signaling and lymphangiogenesis by different mechanisms, which are mediated independently by the two domains of CCBE1: by enhancing the cleavage activity of ADAMTS3 and by facilitating the colocalization of VEGF-C and ADAMTS3. These new insights should be valuable in developing new strategies to therapeutically target VEGF-C/VEGFR-3-induced lymphangiogenesis.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Jha</LastName><ForeName>Sawan Kumar</ForeName><Initials>SK</Initials><Identifier Source="ORCID">http://orcid.org/0000-0003-1898-4928</Identifier><AffiliationInfo><Affiliation>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014, Finland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rauniyar</LastName><ForeName>Khushbu</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014, Finland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Karpanen</LastName><ForeName>Terhi</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>University Hospital Radiumhospitalet and K. G. Jebsen Center for Cancer Immunotherapy, Institute for Clinical Medicine, University of Oslo, Oslo, Norway.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Leppänen</LastName><ForeName>Veli-Matti</ForeName><Initials>VM</Initials><AffiliationInfo><Affiliation>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014, Finland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Wihuri Research Institute, Biomedicum Helsinki, University of Helsinki, Helsinki, Finland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Brouillard</LastName><ForeName>Pascal</ForeName><Initials>P</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-9548-8229</Identifier><AffiliationInfo><Affiliation>de Duve Institute, University of Louvain, Brussels, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vikkula</LastName><ForeName>Miikka</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>de Duve Institute, University of Louvain, Brussels, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Walloon Excellence in Life Sciences and Biotechnology (WELBIO), University of Louvain, Brussels, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Alitalo</LastName><ForeName>Kari</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014, Finland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Wihuri Research Institute, Biomedicum Helsinki, University of Helsinki, Helsinki, Finland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Helsinki University Central Hospital, Helsinki, Finland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jeltsch</LastName><ForeName>Michael</ForeName><Initials>M</Initials><Identifier Source="ORCID">http://orcid.org/0000-0003-2890-7790</Identifier><AffiliationInfo><Affiliation>Translational Cancer Biology Research Program, Biomedicum Helsinki, University of Helsinki, PO Box 63, Haartmaninkatu 8, Helsinki, 00014, Finland. michael@jeltsch.org.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Wihuri Research Institute, Biomedicum Helsinki, University of Helsinki, Helsinki, Finland. michael@jeltsch.org.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>ERC_268804</GrantID><Agency>European Research Council</Agency><Country>International</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate 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PubStatus="accepted"><Year>2017</Year><Month>05</Month><Day>23</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2017</Year><Month>7</Month><Day>9</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2017</Year><Month>7</Month><Day>9</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2017</Year><Month>7</Month><Day>9</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">28687807</ArticleId><ArticleId IdType="doi">10.1038/s41598-017-04982-1</ArticleId><ArticleId IdType="pii">10.1038/s41598-017-04982-1</ArticleId><ArticleId IdType="pmc">PMC5501841</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Belgique</li><li>Finlande</li><li>Norvège</li></country><region><li>Région de Bruxelles-Capitale</li><li>Uusimaa</li><li>Østlandet</li></region><settlement><li>Bruxelles</li><li>Helsinki</li><li>Oslo</li></settlement><orgName><li>Université d'Helsinki</li></orgName></list><tree><country name="Finlande"><region name="Uusimaa"><name sortKey="Jha, Sawan Kumar" sort="Jha, Sawan Kumar" uniqKey="Jha S" first="Sawan Kumar" last="Jha">Sawan Kumar Jha</name></region><name sortKey="Alitalo, Kari" sort="Alitalo, Kari" uniqKey="Alitalo K" first="Kari" last="Alitalo">Kari Alitalo</name><name sortKey="Jeltsch, Michael" sort="Jeltsch, Michael" uniqKey="Jeltsch M" first="Michael" last="Jeltsch">Michael Jeltsch</name><name sortKey="Lepp Nen, Veli Matti" sort="Lepp Nen, Veli Matti" uniqKey="Lepp Nen V" first="Veli-Matti" last="Lepp Nen">Veli-Matti Lepp Nen</name><name sortKey="Rauniyar, Khushbu" sort="Rauniyar, Khushbu" uniqKey="Rauniyar K" first="Khushbu" last="Rauniyar">Khushbu Rauniyar</name></country><country name="Norvège"><region name="Østlandet"><name sortKey="Karpanen, Terhi" sort="Karpanen, Terhi" uniqKey="Karpanen T" first="Terhi" last="Karpanen">Terhi Karpanen</name></region></country><country name="Belgique"><region name="Région de Bruxelles-Capitale"><name sortKey="Brouillard, Pascal" sort="Brouillard, Pascal" uniqKey="Brouillard P" first="Pascal" last="Brouillard">Pascal Brouillard</name></region><name sortKey="Vikkula, Miikka" sort="Vikkula, Miikka" uniqKey="Vikkula M" first="Miikka" last="Vikkula">Miikka Vikkula</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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