Dynamic trafficking and turnover of JAM-C is essential for endothelial cell migration
Identifieur interne : 000868 ( Main/Exploration ); précédent : 000867; suivant : 000869Dynamic trafficking and turnover of JAM-C is essential for endothelial cell migration
Auteurs : Katja B. Kostelnik [Royaume-Uni] ; Amy Barker [Royaume-Uni] ; Christopher Schultz [Royaume-Uni] ; Tom P. Mitchell [Royaume-Uni] ; Vinothini Rajeeve [Royaume-Uni] ; Ian J. White [Royaume-Uni] ; Michel Aurrand-Lions [France] ; Sussan Nourshargh [Royaume-Uni] ; Pedro Cutillas [Royaume-Uni] ; Thomas D. Nightingale [Royaume-Uni]Source :
- PLoS Biology [ 1544-9173 ] ; 2019.
Abstract
Junctional complexes between endothelial cells form a dynamic barrier that hinders passive diffusion of blood constituents into interstitial tissues. Remodelling of junctions is an essential process during leukocyte trafficking, vascular permeability, and angiogenesis. However, for many junctional proteins, the mechanisms of junctional remodelling have yet to be determined. Here, we used receptor mutagenesis, horseradish peroxidase (HRP), and ascorbate peroxidase 2 (APEX-2) proximity labelling, alongside light and electron microscopy (EM), to map the intracellular trafficking routes of junctional adhesion molecule-C (JAM-C). We found that JAM-C cotraffics with receptors associated with changes in permeability such as vascular endothelial cadherin (VE-Cadherin) and neuropilin (NRP)-1 and 2, but not with junctional proteins associated with the transmigration of leukocytes. Dynamic JAM-C trafficking and degradation are necessary for junctional remodelling during cell migration and angiogenesis. By identifying new potential trafficking machinery, we show that a key point of regulation is the ubiquitylation of JAM-C by the E3 ligase Casitas B-lineage lymphoma (CBL), which controls the rate of trafficking versus lysosomal degradation.
Url:
DOI: 10.1371/journal.pbio.3000554
PubMed: 31790392
PubMed Central: 6907879
Affiliations:
- France, Royaume-Uni
- Angleterre, Grand Londres, Provence-Alpes-Côte d'Azur
- Londres, Marseille
- University College de Londres, Université de Londres
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Kostelnik</name><affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Centre for Microvascular Research, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Centre for Microvascular Research, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName><orgName type="university">Université de Londres</orgName></affiliation></author><author><name sortKey="Barker, Amy" sort="Barker, Amy" uniqKey="Barker A" first="Amy" last="Barker">Amy Barker</name><affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Centre for Microvascular Research, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Centre for Microvascular Research, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName><orgName type="university">Université de Londres</orgName></affiliation></author><author><name sortKey="Schultz, Christopher" sort="Schultz, Christopher" uniqKey="Schultz C" first="Christopher" last="Schultz">Christopher Schultz</name><affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Centre for Microvascular Research, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Centre for Microvascular Research, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName><orgName type="university">Université de Londres</orgName></affiliation></author><author><name sortKey="Mitchell, Tom P" sort="Mitchell, Tom P" uniqKey="Mitchell T" first="Tom P." last="Mitchell">Tom P. Mitchell</name><affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Centre for Microvascular Research, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Centre for Microvascular Research, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName><orgName type="university">Université de Londres</orgName></affiliation></author><author><name sortKey="Rajeeve, Vinothini" sort="Rajeeve, Vinothini" uniqKey="Rajeeve V" first="Vinothini" last="Rajeeve">Vinothini Rajeeve</name><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Cell Signalling & Proteomics Group, Barts Cancer Institute, Queen Mary University of London, London, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Cell Signalling & Proteomics Group, Barts Cancer Institute, Queen Mary University of London, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName><orgName type="university">Université de Londres</orgName></affiliation></author><author><name sortKey="White, Ian J" sort="White, Ian J" uniqKey="White I" first="Ian J." last="White">Ian J. White</name><affiliation wicri:level="4"><nlm:aff id="aff003"><addr-line>MRC Laboratory of Molecular Cell Biology, University College London, London, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>MRC Laboratory of Molecular Cell Biology, University College London, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName><orgName type="university">University College de Londres</orgName></affiliation></author><author><name sortKey="Aurrand Lions, Michel" sort="Aurrand Lions, Michel" uniqKey="Aurrand Lions M" first="Michel" last="Aurrand-Lions">Michel Aurrand-Lions</name><affiliation wicri:level="3"><nlm:aff id="aff004"><addr-line>Aix Marseille University, CNRS, INSERM, Institut Paoli-Calmettes, CRCM, Marseille, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Aix Marseille University, CNRS, INSERM, Institut Paoli-Calmettes, CRCM, Marseille</wicri:regionArea><placeName><region type="region">Provence-Alpes-Côte d'Azur</region><region type="old region">Provence-Alpes-Côte d'Azur</region><settlement type="city">Marseille</settlement></placeName></affiliation></author><author><name sortKey="Nourshargh, Sussan" sort="Nourshargh, Sussan" uniqKey="Nourshargh S" first="Sussan" last="Nourshargh">Sussan Nourshargh</name><affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Centre for Microvascular Research, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Centre for Microvascular Research, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName><orgName type="university">Université de Londres</orgName></affiliation></author><author><name sortKey="Cutillas, Pedro" sort="Cutillas, Pedro" uniqKey="Cutillas P" first="Pedro" last="Cutillas">Pedro Cutillas</name><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Cell Signalling & Proteomics Group, Barts Cancer Institute, Queen Mary University of London, London, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Cell Signalling & Proteomics Group, Barts Cancer Institute, Queen Mary University of London, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName><orgName type="university">Université de Londres</orgName></affiliation></author><author><name sortKey="Nightingale, Thomas D" sort="Nightingale, Thomas D" uniqKey="Nightingale T" first="Thomas D." last="Nightingale">Thomas D. Nightingale</name><affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Centre for Microvascular Research, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Centre for Microvascular Research, William Harvey Research Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName><orgName type="university">Université de Londres</orgName></affiliation></author></analytic><series><title level="j">PLoS Biology</title><idno type="ISSN">1544-9173</idno><idno type="eISSN">1545-7885</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Junctional complexes between endothelial cells form a dynamic barrier that hinders passive diffusion of blood constituents into interstitial tissues. Remodelling of junctions is an essential process during leukocyte trafficking, vascular permeability, and angiogenesis. However, for many junctional proteins, the mechanisms of junctional remodelling have yet to be determined. Here, we used receptor mutagenesis, horseradish peroxidase (HRP), and ascorbate peroxidase 2 (APEX-2) proximity labelling, alongside light and electron microscopy (EM), to map the intracellular trafficking routes of junctional adhesion molecule-C (JAM-C). We found that JAM-C cotraffics with receptors associated with changes in permeability such as vascular endothelial cadherin (VE-Cadherin) and neuropilin (NRP)-1 and 2, but not with junctional proteins associated with the transmigration of leukocytes. Dynamic JAM-C trafficking and degradation are necessary for junctional remodelling during cell migration and angiogenesis. By identifying new potential trafficking machinery, we show that a key point of regulation is the ubiquitylation of JAM-C by the E3 ligase Casitas B-lineage lymphoma (CBL), which controls the rate of trafficking versus lysosomal degradation.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Zihni, C" uniqKey="Zihni C">C Zihni</name></author><author><name sortKey="Mills, C" uniqKey="Mills C">C Mills</name></author><author><name sortKey="Matter, K" uniqKey="Matter K">K Matter</name></author><author><name sortKey="Balda, Ms" uniqKey="Balda M">MS Balda</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nourshargh, S" uniqKey="Nourshargh S">S Nourshargh</name></author><author><name sortKey="Alon, R" uniqKey="Alon R">R Alon</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ramasamy, Sk" uniqKey="Ramasamy S">SK Ramasamy</name></author><author><name sortKey="Kusumbe, Ap" uniqKey="Kusumbe A">AP Kusumbe</name></author><author><name sortKey="Adams, Rh" uniqKey="Adams R">RH Adams</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Godo, S" uniqKey="Godo S">S Godo</name></author><author><name sortKey="Shimokawa, H" uniqKey="Shimokawa H">H Shimokawa</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Malinova, Ts" uniqKey="Malinova T">TS Malinova</name></author><author><name sortKey="Huveneers, S" uniqKey="Huveneers S">S Huveneers</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ebnet, K" uniqKey="Ebnet K">K. 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sortKey="Solari, R" uniqKey="Solari R">R Solari</name></author><author><name sortKey="Cutler, Df" uniqKey="Cutler D">DF Cutler</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Michaux, G" uniqKey="Michaux G">G Michaux</name></author><author><name sortKey="Abbitt, Kb" uniqKey="Abbitt K">KB Abbitt</name></author><author><name sortKey="Collinson, Lm" uniqKey="Collinson L">LM Collinson</name></author><author><name sortKey="Haberichter, Sl" uniqKey="Haberichter S">SL Haberichter</name></author><author><name sortKey="Norman, Ke" uniqKey="Norman K">KE Norman</name></author><author><name sortKey="Cutler, Df" uniqKey="Cutler D">DF Cutler</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Carpenter, Ae" uniqKey="Carpenter A">AE Carpenter</name></author><author><name sortKey="Jones, Tr" uniqKey="Jones T">TR Jones</name></author><author><name sortKey="Lamprecht, Mr" uniqKey="Lamprecht M">MR Lamprecht</name></author><author><name sortKey="Clarke, C" uniqKey="Clarke C">C Clarke</name></author><author><name sortKey="Kang, Ih" uniqKey="Kang I">IH Kang</name></author><author><name sortKey="Friman, O" uniqKey="Friman O">O Friman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Casado, P" uniqKey="Casado P">P Casado</name></author><author><name sortKey="Rodriguez Prados, Jc" uniqKey="Rodriguez Prados J">JC Rodriguez-Prados</name></author><author><name sortKey="Cosulich, Sc" uniqKey="Cosulich S">SC Cosulich</name></author><author><name sortKey="Guichard, S" uniqKey="Guichard S">S Guichard</name></author><author><name sortKey="Vanhaesebroeck, B" uniqKey="Vanhaesebroeck B">B Vanhaesebroeck</name></author><author><name sortKey="Joel, S" uniqKey="Joel S">S Joel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rajeeve, V" uniqKey="Rajeeve V">V Rajeeve</name></author><author><name sortKey="Vendrell, I" uniqKey="Vendrell I">I Vendrell</name></author><author><name sortKey="Wilkes, E" uniqKey="Wilkes E">E Wilkes</name></author><author><name sortKey="Torbett, N" uniqKey="Torbett N">N Torbett</name></author><author><name sortKey="Cutillas, Pr" uniqKey="Cutillas P">PR Cutillas</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lui Roberts, Ww" uniqKey="Lui Roberts W">WW Lui-Roberts</name></author><author><name sortKey="Collinson, Lm" uniqKey="Collinson L">LM Collinson</name></author><author><name sortKey="Hewlett, Lj" uniqKey="Hewlett L">LJ Hewlett</name></author><author><name sortKey="Michaux, G" uniqKey="Michaux G">G Michaux</name></author><author><name sortKey="Cutler, Df" uniqKey="Cutler D">DF Cutler</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Schindelin, J" uniqKey="Schindelin J">J Schindelin</name></author><author><name sortKey="Arganda Carreras, I" uniqKey="Arganda Carreras I">I Arganda-Carreras</name></author><author><name sortKey="Frise, E" uniqKey="Frise E">E Frise</name></author><author><name sortKey="Kaynig, V" uniqKey="Kaynig V">V Kaynig</name></author><author><name sortKey="Longair, M" uniqKey="Longair M">M Longair</name></author><author><name sortKey="Pietzsch, T" uniqKey="Pietzsch T">T Pietzsch</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>France</li><li>Royaume-Uni</li></country><region><li>Angleterre</li><li>Grand Londres</li><li>Provence-Alpes-Côte d'Azur</li></region><settlement><li>Londres</li><li>Marseille</li></settlement><orgName><li>University College de Londres</li><li>Université de Londres</li></orgName></list><tree><country name="Royaume-Uni"><region name="Angleterre"><name sortKey="Kostelnik, Katja B" sort="Kostelnik, Katja B" uniqKey="Kostelnik K" first="Katja B." last="Kostelnik">Katja B. Kostelnik</name></region><name sortKey="Barker, Amy" sort="Barker, Amy" uniqKey="Barker A" first="Amy" last="Barker">Amy Barker</name><name sortKey="Cutillas, Pedro" sort="Cutillas, Pedro" uniqKey="Cutillas P" first="Pedro" last="Cutillas">Pedro Cutillas</name><name sortKey="Mitchell, Tom P" sort="Mitchell, Tom P" uniqKey="Mitchell T" first="Tom P." last="Mitchell">Tom P. Mitchell</name><name sortKey="Nightingale, Thomas D" sort="Nightingale, Thomas D" uniqKey="Nightingale T" first="Thomas D." last="Nightingale">Thomas D. Nightingale</name><name sortKey="Nourshargh, Sussan" sort="Nourshargh, Sussan" uniqKey="Nourshargh S" first="Sussan" last="Nourshargh">Sussan Nourshargh</name><name sortKey="Rajeeve, Vinothini" sort="Rajeeve, Vinothini" uniqKey="Rajeeve V" first="Vinothini" last="Rajeeve">Vinothini Rajeeve</name><name sortKey="Schultz, Christopher" sort="Schultz, Christopher" uniqKey="Schultz C" first="Christopher" last="Schultz">Christopher Schultz</name><name sortKey="White, Ian J" sort="White, Ian J" uniqKey="White I" first="Ian J." last="White">Ian J. White</name></country><country name="France"><region name="Provence-Alpes-Côte d'Azur"><name sortKey="Aurrand Lions, Michel" sort="Aurrand Lions, Michel" uniqKey="Aurrand Lions M" first="Michel" last="Aurrand-Lions">Michel Aurrand-Lions</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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