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 : 000595 ( Main/Exploration ); précédent : 000594; suivant : 000596Efficient 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
Url:
DOI: 10.1038/s41598-017-04982-1
PubMed: 28687807
PubMed Central: 5501841
Affiliations:
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Haartmaninkatu 8, Helsinki, 00014 Finland</nlm:aff><country xml:lang="fr">Finlande</country><wicri:regionArea>PO Box 63, Haartmaninkatu 8, Helsinki</wicri:regionArea><wicri:noRegion>Helsinki</wicri:noRegion></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:aff id="Aff4">University Hospital Radiumhospitalet and K. G. Jebsen Center for Cancer Immunotherapy, Institute for Clinical Medicine, University of Oslo, Oslo, Norway</nlm:aff><country xml:lang="fr">Norvège</country><wicri:regionArea>University Hospital Radiumhospitalet and K. G. 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Helsinki</wicri:regionArea><wicri:noRegion>Helsinki</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0410 2071</institution-id><institution-id institution-id-type="GRID">grid.7737.4</institution-id><institution>Wihuri Research Institute,</institution><institution>Biomedicum Helsinki, University of Helsinki,</institution></institution-wrap>Helsinki, Finland</nlm:aff><country xml:lang="fr">Finlande</country><wicri:regionArea>Helsinki</wicri:regionArea></affiliation></author><author><name sortKey="Brouillard, Pascal" sort="Brouillard, Pascal" uniqKey="Brouillard P" first="Pascal" last="Brouillard">Pascal Brouillard</name><affiliation wicri:level="1"><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2294 713X</institution-id><institution-id institution-id-type="GRID">grid.7942.8</institution-id><institution>de Duve 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8, Helsinki</wicri:regionArea><wicri:noRegion>Helsinki</wicri:noRegion><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName><orgName type="university">Université d'Helsinki</orgName></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0410 2071</institution-id><institution-id institution-id-type="GRID">grid.7737.4</institution-id><institution>Wihuri Research Institute,</institution><institution>Biomedicum Helsinki, University of Helsinki,</institution></institution-wrap>Helsinki, Finland</nlm:aff><country xml:lang="fr">Finlande</country><wicri:regionArea>Helsinki</wicri:regionArea><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName><orgName type="university">Université d'Helsinki</orgName></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9950 5666</institution-id><institution-id institution-id-type="GRID">grid.15485.3d</institution-id><institution></institution><institution>Helsinki University Central Hospital,</institution></institution-wrap>Helsinki, Finland</nlm:aff><country xml:lang="fr">Finlande</country><wicri:regionArea>Helsinki</wicri:regionArea><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="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0410 2071</institution-id><institution-id institution-id-type="GRID">grid.7737.4</institution-id><institution>Translational Cancer Biology Research Program,</institution><institution>Biomedicum Helsinki, University of Helsinki,</institution></institution-wrap>PO Box 63, Haartmaninkatu 8, Helsinki, 00014 Finland</nlm:aff><country xml:lang="fr">Finlande</country><wicri:regionArea>PO Box 63, Haartmaninkatu 8, Helsinki</wicri:regionArea><wicri:noRegion>Helsinki</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0410 2071</institution-id><institution-id institution-id-type="GRID">grid.7737.4</institution-id><institution>Wihuri Research Institute,</institution><institution>Biomedicum Helsinki, University of Helsinki,</institution></institution-wrap>Helsinki, Finland</nlm:aff><country xml:lang="fr">Finlande</country><wicri:regionArea>Helsinki</wicri:regionArea></affiliation></author></analytic><series><title level="j">Scientific Reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p id="Par1">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 <italic>in vitro</italic> 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.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Alitalo, K" uniqKey="Alitalo K">K Alitalo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Krebs, R" uniqKey="Krebs R">R Krebs</name></author><author><name sortKey="Jeltsch, M" uniqKey="Jeltsch M">M Jeltsch</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Krebs, R" uniqKey="Krebs R">R Krebs</name></author><author><name sortKey="Jeltsch, M" uniqKey="Jeltsch M">M Jeltsch</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Joukov, V" uniqKey="Joukov V">V Joukov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Villefranc, Ja" uniqKey="Villefranc J">JA Villefranc</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Balboa Beltran, E" uniqKey="Balboa Beltran E">E Balboa-Beltran</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Keskitalo, S" uniqKey="Keskitalo S">S Keskitalo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Karkkainen, Mj" uniqKey="Karkkainen M">MJ Karkkainen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gordon, K" uniqKey="Gordon K">K Gordon</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Alders, M" uniqKey="Alders M">M Alders</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bui, Hm" uniqKey="Bui H">HM Bui</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bos, Fl" uniqKey="Bos F">FL Bos</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Karkkainen, Mj" uniqKey="Karkkainen M">MJ Karkkainen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Alders, M" uniqKey="Alders M">M Alders</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Roukens, Mg" uniqKey="Roukens M">MG Roukens</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jeltsch, M" uniqKey="Jeltsch M">M Jeltsch</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Janssen, L" uniqKey="Janssen L">L Janssen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Johns, Sc" uniqKey="Johns S">SC Johns</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Facucho Oliveira, J" uniqKey="Facucho Oliveira J">J Facucho-Oliveira</name></author><author><name sortKey="Bento, M" uniqKey="Bento M">M Bento</name></author><author><name sortKey="Belo, J" uniqKey="Belo J">J Belo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hasselhof, V" uniqKey="Hasselhof V">V Hasselhof</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nelson, Gm" uniqKey="Nelson G">GM Nelson</name></author><author><name sortKey="Padera, Tp" uniqKey="Padera T">TP Padera</name></author><author><name sortKey="Garkavtsev, I" uniqKey="Garkavtsev I">I Garkavtsev</name></author><author><name sortKey="Shioda, T" uniqKey="Shioda T">T Shioda</name></author><author><name sortKey="Jain, Rk" uniqKey="Jain R">RK Jain</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Riaz, M" uniqKey="Riaz M">M Riaz</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lek, M" uniqKey="Lek M">M Lek</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hogan, Bm" uniqKey="Hogan B">BM Hogan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zhang, X" uniqKey="Zhang X">X Zhang</name></author><author><name sortKey="Groopman, Je" uniqKey="Groopman J">JE Groopman</name></author><author><name sortKey="Wang, Jf" uniqKey="Wang J">JF Wang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wang, Jf" uniqKey="Wang J">JF Wang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ruhrberg, C" uniqKey="Ruhrberg C">C Ruhrberg</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gerhardt, H" uniqKey="Gerhardt H">H Gerhardt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mccoll, Bk" uniqKey="Mccoll B">BK McColl</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tortorella, M" uniqKey="Tortorella M">M Tortorella</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lotta, La" uniqKey="Lotta L">LA Lotta</name></author><author><name sortKey="Garagiola, I" uniqKey="Garagiola I">I Garagiola</name></author><author><name sortKey="Palla, R" uniqKey="Palla R">R Palla</name></author><author><name sortKey="Cairo, A" uniqKey="Cairo A">A Cairo</name></author><author><name sortKey="Peyvandi, F" uniqKey="Peyvandi F">F Peyvandi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lieu, Ch" uniqKey="Lieu C">CH Lieu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Achen, Mg" uniqKey="Achen M">MG Achen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="M Kinen, T" uniqKey="M Kinen T">T Mäkinen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Baluk, P" uniqKey="Baluk P">P Baluk</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tammela, T" uniqKey="Tammela T">T Tammela</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Leppanen, V M" uniqKey="Leppanen V">V-M Leppanen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hakanpaa, L" uniqKey="Hakanpaa L">L Hakanpaa</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Belgique</li><li>Finlande</li><li>Norvège</li></country><region><li>Uusimaa</li><li>Østlandet</li></region><settlement><li>Helsinki</li><li>Oslo</li></settlement><orgName><li>Université d'Helsinki</li></orgName></list><tree><country name="Finlande"><noRegion><name sortKey="Jha, Sawan Kumar" sort="Jha, Sawan Kumar" uniqKey="Jha S" first="Sawan Kumar" last="Jha">Sawan Kumar Jha</name></noRegion><name sortKey="Alitalo, Kari" sort="Alitalo, Kari" uniqKey="Alitalo K" first="Kari" last="Alitalo">Kari Alitalo</name><name sortKey="Alitalo, Kari" sort="Alitalo, Kari" uniqKey="Alitalo K" first="Kari" last="Alitalo">Kari Alitalo</name><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="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="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"><noRegion><name sortKey="Brouillard, Pascal" sort="Brouillard, Pascal" uniqKey="Brouillard P" first="Pascal" last="Brouillard">Pascal Brouillard</name></noRegion><name sortKey="Vikkula, Miikka" sort="Vikkula, Miikka" uniqKey="Vikkula M" first="Miikka" last="Vikkula">Miikka Vikkula</name><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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