Force tuning through regulation of clathrin-dependent integrin endocytosis
Integrin endocytosis is essential for many fundamental cellular processes. Whether and how the internalization impacts cellular mechanics remains elusive. Whereas previous studies reported the contribution of the integrin activator, talin, in force development, the involvement of inhibitors is less...
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| Veröffentlicht in: | The Journal of cell biology 2023-01, Vol.222 (1), p.1 |
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| creator | Kyumurkov, Alexander Bouin, Anne-Pascale Boissan, Mathieu Manet, Sandra Baschieri, Francesco Proponnet-Guerault, Mathilde Balland, Martial Destaing, Olivier Régent-Kloeckner, Myriam Calmel, Claire Nicolas, Alice Waharte, François Chavrier, Philippe Montagnac, Guillaume Planus, Emmanuelle Albiges-Rizo, Corinne |
| description | Integrin endocytosis is essential for many fundamental cellular processes. Whether and how the internalization impacts cellular mechanics remains elusive. Whereas previous studies reported the contribution of the integrin activator, talin, in force development, the involvement of inhibitors is less documented. We identified ICAP-1 as an integrin inhibitor involved in mechanotransduction by co-working with NME2 to control clathrin-mediated endocytosis of integrins at the edge of focal adhesions (FA). Loss of ICAP-1 enables β3-integrin-mediated force generation independently of β1 integrin. β3-integrin-mediated forces were associated with a decrease in β3 integrin dynamics stemming from their reduced diffusion within adhesion sites and slow turnover of FA. The decrease in β3 integrin dynamics correlated with a defect in integrin endocytosis. ICAP-1 acts as an adaptor for clathrin-dependent endocytosis of integrins. ICAP-1 controls integrin endocytosis by interacting with NME2, a key regulator of dynamin-dependent clathrin-coated pits fission. Control of clathrin-mediated integrin endocytosis by an inhibitor is an unprecedented mechanism to tune forces at FA. |
| doi_str_mv | 10.1083/jcb.202004025 |
| format | Article |
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Whether and how the internalization impacts cellular mechanics remains elusive. Whereas previous studies reported the contribution of the integrin activator, talin, in force development, the involvement of inhibitors is less documented. We identified ICAP-1 as an integrin inhibitor involved in mechanotransduction by co-working with NME2 to control clathrin-mediated endocytosis of integrins at the edge of focal adhesions (FA). Loss of ICAP-1 enables β3-integrin-mediated force generation independently of β1 integrin. β3-integrin-mediated forces were associated with a decrease in β3 integrin dynamics stemming from their reduced diffusion within adhesion sites and slow turnover of FA. The decrease in β3 integrin dynamics correlated with a defect in integrin endocytosis. ICAP-1 acts as an adaptor for clathrin-dependent endocytosis of integrins. ICAP-1 controls integrin endocytosis by interacting with NME2, a key regulator of dynamin-dependent clathrin-coated pits fission. Control of clathrin-mediated integrin endocytosis by an inhibitor is an unprecedented mechanism to tune forces at FA.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.202004025</identifier><identifier>PMID: 36250940</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Adhesion ; Biophysics ; Clathrin ; Clathrin - metabolism ; Coated pits ; Diffusion rate ; Dynamin ; Endocytosis ; Endocytosis - physiology ; Focal Adhesions ; Integrin beta1 - genetics ; Integrin beta3 ; Integrins ; Internalization ; Life Sciences ; Mechanotransduction ; Mechanotransduction, Cellular ; Talin ; Talin - genetics</subject><ispartof>The Journal of cell biology, 2023-01, Vol.222 (1), p.1</ispartof><rights>2022 Kyumurkov et al.</rights><rights>Copyright Rockefeller University Press Jan 2023</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2022 Kyumurkov et al. 2022 Kyumurkov et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c449t-8146b8f629bee5a4c97377cfeb20f203d2b6b767f25cd649a3847b1ed7ce9c7a3</citedby><cites>FETCH-LOGICAL-c449t-8146b8f629bee5a4c97377cfeb20f203d2b6b767f25cd649a3847b1ed7ce9c7a3</cites><orcidid>0000-0002-7351-733X ; 0000-0001-7622-3700 ; 0000-0002-6585-9735 ; 0000-0002-9616-6173 ; 0000-0003-1758-1174 ; 0000-0001-6855-4446 ; 0000-0003-0218-5320 ; 0000-0002-6333-4150 ; 0000-0002-3981-906X ; 0000-0001-6494-5722</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36250940$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03834328$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Kyumurkov, Alexander</creatorcontrib><creatorcontrib>Bouin, Anne-Pascale</creatorcontrib><creatorcontrib>Boissan, Mathieu</creatorcontrib><creatorcontrib>Manet, Sandra</creatorcontrib><creatorcontrib>Baschieri, Francesco</creatorcontrib><creatorcontrib>Proponnet-Guerault, Mathilde</creatorcontrib><creatorcontrib>Balland, Martial</creatorcontrib><creatorcontrib>Destaing, Olivier</creatorcontrib><creatorcontrib>Régent-Kloeckner, Myriam</creatorcontrib><creatorcontrib>Calmel, Claire</creatorcontrib><creatorcontrib>Nicolas, Alice</creatorcontrib><creatorcontrib>Waharte, François</creatorcontrib><creatorcontrib>Chavrier, Philippe</creatorcontrib><creatorcontrib>Montagnac, Guillaume</creatorcontrib><creatorcontrib>Planus, Emmanuelle</creatorcontrib><creatorcontrib>Albiges-Rizo, Corinne</creatorcontrib><title>Force tuning through regulation of clathrin-dependent integrin endocytosis</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>Integrin endocytosis is essential for many fundamental cellular processes. Whether and how the internalization impacts cellular mechanics remains elusive. Whereas previous studies reported the contribution of the integrin activator, talin, in force development, the involvement of inhibitors is less documented. We identified ICAP-1 as an integrin inhibitor involved in mechanotransduction by co-working with NME2 to control clathrin-mediated endocytosis of integrins at the edge of focal adhesions (FA). Loss of ICAP-1 enables β3-integrin-mediated force generation independently of β1 integrin. β3-integrin-mediated forces were associated with a decrease in β3 integrin dynamics stemming from their reduced diffusion within adhesion sites and slow turnover of FA. The decrease in β3 integrin dynamics correlated with a defect in integrin endocytosis. ICAP-1 acts as an adaptor for clathrin-dependent endocytosis of integrins. ICAP-1 controls integrin endocytosis by interacting with NME2, a key regulator of dynamin-dependent clathrin-coated pits fission. Control of clathrin-mediated integrin endocytosis by an inhibitor is an unprecedented mechanism to tune forces at FA.</description><subject>Adhesion</subject><subject>Biophysics</subject><subject>Clathrin</subject><subject>Clathrin - metabolism</subject><subject>Coated pits</subject><subject>Diffusion rate</subject><subject>Dynamin</subject><subject>Endocytosis</subject><subject>Endocytosis - physiology</subject><subject>Focal Adhesions</subject><subject>Integrin beta1 - genetics</subject><subject>Integrin beta3</subject><subject>Integrins</subject><subject>Internalization</subject><subject>Life Sciences</subject><subject>Mechanotransduction</subject><subject>Mechanotransduction, Cellular</subject><subject>Talin</subject><subject>Talin - genetics</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkcGP1CAUxonRuOPq0atp4kUPXR8PKHAx2WxcVzOJFz2TltKWSQdGaDfZ_14ms050Tzze-_HxwUfIWwpXFBT7tLPdFQICcEDxjGyo4FAryuE52QAgrbVAcUFe5byDAknOXpIL1qAAzWFDvt_GZF21rMGHsVqmFNdxqpIb17ldfAxVHCpbyin5UPfu4ELvwlL5sLixtKqyj_Zhidnn1-TF0M7ZvXlcL8mv2y8_b-7q7Y-v326ut7XlXC9Hb02nhgZ155xoudWSSWkH1yEMCKzHrulkIwcUtm-4bpnisqOul9ZpK1t2ST6fdA9rt3e9LX5SO5tD8vs2PZjYevP_JPjJjPHeaCG1Vk0R-HgSmJ4cu7vemmMPmGKcobqnhf3weFmKv1eXF7P32bp5boOLazYoUXCOSLGg75-gu7imUL6iUA0oJZAfBesTZVPMObnh7ICCOSZqSqLmnGjh3_372jP9N0L2B23hnKM</recordid><startdate>20230102</startdate><enddate>20230102</enddate><creator>Kyumurkov, Alexander</creator><creator>Bouin, Anne-Pascale</creator><creator>Boissan, Mathieu</creator><creator>Manet, Sandra</creator><creator>Baschieri, Francesco</creator><creator>Proponnet-Guerault, Mathilde</creator><creator>Balland, Martial</creator><creator>Destaing, Olivier</creator><creator>Régent-Kloeckner, Myriam</creator><creator>Calmel, Claire</creator><creator>Nicolas, Alice</creator><creator>Waharte, François</creator><creator>Chavrier, Philippe</creator><creator>Montagnac, Guillaume</creator><creator>Planus, Emmanuelle</creator><creator>Albiges-Rizo, Corinne</creator><general>Rockefeller University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-7351-733X</orcidid><orcidid>https://orcid.org/0000-0001-7622-3700</orcidid><orcidid>https://orcid.org/0000-0002-6585-9735</orcidid><orcidid>https://orcid.org/0000-0002-9616-6173</orcidid><orcidid>https://orcid.org/0000-0003-1758-1174</orcidid><orcidid>https://orcid.org/0000-0001-6855-4446</orcidid><orcidid>https://orcid.org/0000-0003-0218-5320</orcidid><orcidid>https://orcid.org/0000-0002-6333-4150</orcidid><orcidid>https://orcid.org/0000-0002-3981-906X</orcidid><orcidid>https://orcid.org/0000-0001-6494-5722</orcidid></search><sort><creationdate>20230102</creationdate><title>Force tuning through regulation of clathrin-dependent integrin endocytosis</title><author>Kyumurkov, Alexander ; 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Whether and how the internalization impacts cellular mechanics remains elusive. Whereas previous studies reported the contribution of the integrin activator, talin, in force development, the involvement of inhibitors is less documented. We identified ICAP-1 as an integrin inhibitor involved in mechanotransduction by co-working with NME2 to control clathrin-mediated endocytosis of integrins at the edge of focal adhesions (FA). Loss of ICAP-1 enables β3-integrin-mediated force generation independently of β1 integrin. β3-integrin-mediated forces were associated with a decrease in β3 integrin dynamics stemming from their reduced diffusion within adhesion sites and slow turnover of FA. The decrease in β3 integrin dynamics correlated with a defect in integrin endocytosis. ICAP-1 acts as an adaptor for clathrin-dependent endocytosis of integrins. ICAP-1 controls integrin endocytosis by interacting with NME2, a key regulator of dynamin-dependent clathrin-coated pits fission. 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| subjects | Adhesion Biophysics Clathrin Clathrin - metabolism Coated pits Diffusion rate Dynamin Endocytosis Endocytosis - physiology Focal Adhesions Integrin beta1 - genetics Integrin beta3 Integrins Internalization Life Sciences Mechanotransduction Mechanotransduction, Cellular Talin Talin - genetics |
| title | Force tuning through regulation of clathrin-dependent integrin endocytosis |
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