{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T23:27:18Z","timestamp":1792106838781,"version":"4.4.0"},"reference-count":95,"publisher":"The Company of Biologists","issue":"10","license":[{"start":{"date-parts":[[2023,5,31]],"date-time":"2023-05-31T00:00:00Z","timestamp":1685491200000},"content-version":"vor","delay-in-days":16,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"crossref","award":["18K07198"],"award-info":[{"award-number":["18K07198"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"crossref","award":["JP22H04926"],"award-info":[{"award-number":["JP22H04926"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"crossref","award":["19H01064"],"award-info":[{"award-number":["19H01064"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"crossref","award":["19H03225"],"award-info":[{"award-number":["19H03225"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"crossref","award":["19KK0180"],"award-info":[{"award-number":["19KK0180"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100016189","name":"Wesco Science Foundation","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100016189","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100012330","name":"Okayama University","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100012330","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,5,15]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>Collective cell migration is the coordinated movement of multiple cells connected by cadherin-based adherens junctions and is essential for physiological and pathological processes. Cadherins undergo dynamic intracellular trafficking, and their surface level is determined by a balance between endocytosis, recycling and degradation. However, the regulatory mechanism of cadherin turnover in collective cell migration remains elusive. In this study, we show that the Bin\/amphiphysin\/Rvs (BAR) domain protein pacsin 2 (protein kinase C and casein kinase substrate in neurons protein 2) plays an essential role in collective cell migration by regulating N-cadherin (also known as CDH2) endocytosis in human cancer cells. Pacsin 2-depleted cells formed cell\u2013cell contacts enriched with N-cadherin and migrated in a directed manner. Furthermore, pacsin 2-depleted cells showed attenuated internalization of N-cadherin from the cell surface. Interestingly, GST pull-down assays demonstrated that the pacsin 2 SH3 domain binds to the cytoplasmic region of N-cadherin, and expression of an N-cadherin mutant defective in binding to pacsin 2 phenocopied pacsin 2 RNAi cells both in cell contact formation and N-cadherin endocytosis. These data support new insights into a novel endocytic route of N-cadherin in collective cell migration, highlighting pacsin 2 as a possible therapeutic target for cancer metastasis.<\/jats:p>","DOI":"10.1242\/jcs.260827","type":"journal-article","created":{"date-parts":[[2023,5,3]],"date-time":"2023-05-03T07:58:42Z","timestamp":1683100722000},"source":"Crossref","is-referenced-by-count":10,"title":["Pacsin 2-dependent N-cadherin internalization regulates the migration behaviour of malignant cancer cells"],"prefix":"10.1242","volume":"136","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2923-878X","authenticated-orcid":false,"given":"Haymar","family":"Wint","sequence":"first","affiliation":[{"name":"Dentistry and Pharmaceutical Sciences 1 Department of Neuroscience, Okayama University Graduate School of Medicine , , Shikata-cho 2-5-1, Kita-ku, Okayama 700-8558 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0580-2606","authenticated-orcid":false,"given":"Jianzhen","family":"Li","sequence":"additional","affiliation":[{"name":"Dentistry and Pharmaceutical Sciences 1 Department of Neuroscience, Okayama University Graduate School of Medicine , , Shikata-cho 2-5-1, Kita-ku, Okayama 700-8558 , Japan"},{"name":"RIKEN Center for Brain Science 2 Laboratory for Neural Cell Dynamics , , Hirosawa 2-1, Wako, Saitama 351-0198 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tadashi","family":"Abe","sequence":"additional","affiliation":[{"name":"Dentistry and Pharmaceutical Sciences 1 Department of Neuroscience, Okayama University Graduate School of Medicine , , Shikata-cho 2-5-1, Kita-ku, Okayama 700-8558 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hiroshi","family":"Yamada","sequence":"additional","affiliation":[{"name":"Dentistry and Pharmaceutical Sciences 1 Department of Neuroscience, Okayama University Graduate School of Medicine , , Shikata-cho 2-5-1, Kita-ku, Okayama 700-8558 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1379-3930","authenticated-orcid":false,"given":"Takumi","family":"Higaki","sequence":"additional","affiliation":[{"name":"Kumamoto University 3 Faculty of Advanced Science and Technology , , Kurokami, Chuo-ku, Kumamoto 860-8555 , Japan"},{"name":", Kumamoto University 4 International Research Organization for Advanced Science and Technology , Kurokami, Chuo-ku, Kumamoto 860-8555 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yasutomo","family":"Nasu","sequence":"additional","affiliation":[{"name":"Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences 5 Department of Urology , , Okayama 700-8558 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masami","family":"Watanabe","sequence":"additional","affiliation":[{"name":"Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences 5 Department of Urology , , Okayama 700-8558 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6555-9425","authenticated-orcid":false,"given":"Kohji","family":"Takei","sequence":"additional","affiliation":[{"name":"Dentistry and Pharmaceutical Sciences 1 Department of Neuroscience, Okayama University Graduate School of Medicine , , Shikata-cho 2-5-1, Kita-ku, Okayama 700-8558 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3183-6551","authenticated-orcid":false,"given":"Tetsuya","family":"Takeda","sequence":"additional","affiliation":[{"name":"Dentistry and Pharmaceutical Sciences 1 Department of Neuroscience, Okayama University Graduate School of Medicine , , Shikata-cho 2-5-1, Kita-ku, Okayama 700-8558 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","published-online":{"date-parts":[[2023,5,31]]},"reference":[{"key":"2023053109142731500_JCS260827C1","doi-asserted-by":"publisher","first-page":"1110","DOI":"10.1016\/j.cell.2014.07.013","article-title":"Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis","volume":"158","author":"Aceto","year":"2014","journal-title":"Cell"},{"key":"2023053109142731500_JCS260827C2","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1091\/mbc.12.4.847","article-title":"Rac1 regulates adherens junctions through endocytosis of E-cadherin","volume":"12","author":"Akhtar","year":"2001","journal-title":"Mol. Biol. Cell"},{"key":"2023053109142731500_JCS260827C3","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1091\/mbc.e04-09-0845","article-title":"Regulation of endocytosis, nuclear translocation, and signaling of fibroblast growth factor receptor 1 by E-cadherin","volume":"16","author":"Bryant","year":"2005","journal-title":"Mol. Biol. Cell"},{"key":"2023053109142731500_JCS260827C4","doi-asserted-by":"publisher","first-page":"1818","DOI":"10.1242\/jcs.000653","article-title":"EGF induces macropinocytosis and SNX1-modulated recycling of E-cadherin","volume":"120","author":"Bryant","year":"2007","journal-title":"J. Cell Sci."},{"key":"2023053109142731500_JCS260827C5","doi-asserted-by":"publisher","first-page":"1262","DOI":"10.1111\/tra.12448","article-title":"Cadherin tales: regulation of cadherin function by endocytic membrane trafficking","volume":"17","author":"Cadwell","year":"2016","journal-title":"Traffic"},{"key":"2023053109142731500_JCS260827C6","doi-asserted-by":"publisher","first-page":"957","DOI":"10.1038\/nature07441","article-title":"Contact inhibition of locomotion in vivo controls neural crest directional migration","volume":"456","author":"Carmona-Fontaine","year":"2008","journal-title":"Nature"},{"key":"2023053109142731500_JCS260827C7","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1158\/2159-8290.CD-12-0095","article-title":"The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data","volume":"2","author":"Cerami","year":"2012","journal-title":"Cancer Discov."},{"key":"2023053109142731500_JCS260827C8","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.ppat.1006070","article-title":"Clostridium difficile Toxin a undergoes clathrin-independent, PACSIN2-dependent endocytosis","volume":"12","author":"Chandrasekaran","year":"2016","journal-title":"PLoS Pathog."},{"key":"2023053109142731500_JCS260827C9","doi-asserted-by":"publisher","first-page":"1337","DOI":"10.1016\/j.febslet.2009.03.037","article-title":"Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins","volume":"583","author":"Chao","year":"2009","journal-title":"FEBS Lett."},{"key":"2023053109142731500_JCS260827C10","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1111\/tra.12473","article-title":"\u03bc2-Dependent endocytosis of N-cadherin is regulated by \u03b2-catenin to facilitate neurite outgrowth","volume":"18","author":"Chen","year":"2017","journal-title":"Traffic"},{"key":"2023053109142731500_JCS260827C11","doi-asserted-by":"publisher","first-page":"1970","DOI":"10.1091\/mbc.e08-07-0735","article-title":"p120-catenin inhibits VE-cadherin internalization through a Rho-independent mechanism","volume":"20","author":"Chiasson","year":"2009","journal-title":"Mol. Biol. Cell"},{"key":"2023053109142731500_JCS260827C12","doi-asserted-by":"publisher","first-page":"4110","DOI":"10.18632\/oncotarget.6588","article-title":"Loss of E-cadherin disrupts ovarian epithelial inclusion cyst formation and collective cell movement in ovarian cancer cells","volume":"7","author":"Choi","year":"2016","journal-title":"Oncotarget"},{"key":"2023053109142731500_JCS260827C13","doi-asserted-by":"publisher","first-page":"1002","DOI":"10.1111\/eci.12683","article-title":"Rab11 collaborates E-cadherin to promote collective cell migration and indicates a poor prognosis in colorectal carcinoma","volume":"46","author":"Chung","year":"2016","journal-title":"Eur. J. Clin. Invest."},{"key":"2023053109142731500_JCS260827C14","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1080\/21541248.2017.1366965","article-title":"Small GTPases orchestrate cell-cell communication during collective cell movement","volume":"11","author":"Combedazou","year":"2020","journal-title":"Small GTPases"},{"key":"2023053109142731500_JCS260827C15","doi-asserted-by":"publisher","first-page":"e55069","DOI":"10.1371\/journal.pone.0055069","article-title":"N-cadherin dependent collective cell invasion of prostate cancer cells is regulated by the N-terminus of alpha-catenin","volume":"8","author":"Cui","year":"2013","journal-title":"PLoS ONE"},{"key":"2023053109142731500_JCS260827C16","doi-asserted-by":"publisher","first-page":"525","DOI":"10.1083\/jcb.200307111","article-title":"A core function for p120-catenin in cadherin turnover","volume":"163","author":"Davis","year":"2003","journal-title":"J. Cell Biol."},{"key":"2023053109142731500_JCS260827C17","doi-asserted-by":"publisher","first-page":"2375","DOI":"10.1242\/jcs.080630","article-title":"The F-BAR domain protein PACSIN2 associates with Rac1 and regulates cell spreading and migration","volume":"124","author":"de Kreuk","year":"2011","journal-title":"J. Cell Sci."},{"key":"2023053109142731500_JCS260827C18","doi-asserted-by":"publisher","first-page":"43438","DOI":"10.1074\/jbc.M112.391078","article-title":"The F-BAR protein PACSIN2 regulates epidermal growth factor receptor internalization","volume":"287","author":"de Kreuk","year":"2012","journal-title":"J. Biol. Chem."},{"key":"2023053109142731500_JCS260827C19","doi-asserted-by":"publisher","first-page":"4272","DOI":"10.1093\/emboj\/19.16.4272","article-title":"Dynamin mediates caveolar sequestration of muscarinic cholinergic receptors and alteration in NO signaling","volume":"19","author":"Dessy","year":"2000","journal-title":"EMBO J."},{"key":"2023053109142731500_JCS260827C20","doi-asserted-by":"publisher","first-page":"12210","DOI":"10.1038\/ncomms12210","article-title":"The F-BAR protein pacsin2 inhibits asymmetric VE-cadherin internalization from tensile adherens junctions","volume":"7","author":"Dorland","year":"2016","journal-title":"Nat. Commun."},{"key":"2023053109142731500_JCS260827C21","doi-asserted-by":"publisher","first-page":"e13783","DOI":"10.1111\/apha.13783","article-title":"PACSIN proteins in vivo: roles in development and physiology","volume":"234","author":"Dumont","year":"2022","journal-title":"Acta Physiol. (Oxf.)"},{"key":"2023053109142731500_JCS260827C22","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1007\/s11010-020-03771-1","article-title":"Molecular and nanoscale evaluation of N-cadherin expression in invasive bladder cancer cells under control conditions or GW501516 exposure","volume":"471","author":"Elie-Caille","year":"2020","journal-title":"Mol. Cell. Biochem."},{"key":"2023053109142731500_JCS260827C23","doi-asserted-by":"publisher","first-page":"581","DOI":"10.1038\/ncb1262","article-title":"Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase","volume":"7","author":"Ezratty","year":"2005","journal-title":"Nat. Cell Biol."},{"key":"2023053109142731500_JCS260827C24","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1038\/nrm2720","article-title":"Collective cell migration in morphogenesis, regeneration and cancer","volume":"10","author":"Friedl","year":"2009","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023053109142731500_JCS260827C25","doi-asserted-by":"publisher","first-page":"100077","DOI":"10.1074\/jbc.RA120.015184","article-title":"Mutant BIN1-Dynamin 2 complexes dysregulate membrane remodeling in the pathogenesis of centronuclear myopathy","volume":"296","author":"Fujise","year":"2021","journal-title":"J. Biol. Chem."},{"key":"2023053109142731500_JCS260827C26","doi-asserted-by":"publisher","first-page":"pl1","DOI":"10.1126\/scisignal.2004088","article-title":"Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal","volume":"6","author":"Gao","year":"2013","journal-title":"Sci. Signal."},{"key":"2023053109142731500_JCS260827C27","doi-asserted-by":"publisher","first-page":"1223","DOI":"10.1038\/ncb1486","article-title":"VEGF controls endothelial-cell permeability by promoting the \u03b2-arrestin-dependent endocytosis of VE-cadherin","volume":"8","author":"Gavard","year":"2006","journal-title":"Nat. Cell Biol."},{"key":"2023053109142731500_JCS260827C28","doi-asserted-by":"publisher","first-page":"622","DOI":"10.1038\/nrm1699","article-title":"Regulation of cadherin-mediated adhesion in morphogenesis","volume":"6","author":"Gumbiner","year":"2005","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023053109142731500_JCS260827C29","doi-asserted-by":"publisher","first-page":"556","DOI":"10.1016\/j.tcb.2015.06.003","article-title":"Collective cell migration: Guidance principles and hierarchies","volume":"25","author":"Haeger","year":"2015","journal-title":"Trends Cell Biol."},{"key":"2023053109142731500_JCS260827C30","doi-asserted-by":"publisher","first-page":"3199","DOI":"10.1101\/gad.1486806","article-title":"Cadherins in development: cell adhesion, sorting, and tissue morphogenesis","volume":"20","author":"Halbleib","year":"2006","journal-title":"Genes Dev."},{"key":"2023053109142731500_JCS260827C31","doi-asserted-by":"publisher","first-page":"533","DOI":"10.1038\/s41568-018-0038-z","article-title":"Every step of the way: integrins in cancer progression and metastasis","volume":"18","author":"Hamidi","year":"2018","journal-title":"Nat. Rev. Cancer"},{"key":"2023053109142731500_JCS260827C32","doi-asserted-by":"publisher","first-page":"2777","DOI":"10.1242\/jcs.084319","article-title":"Pacsin 2 is recruited to caveolae and functions in caveolar biogenesis","volume":"124","author":"Hansen","year":"2011","journal-title":"J. Cell Sci."},{"key":"2023053109142731500_JCS260827C33","doi-asserted-by":"publisher","first-page":"1311","DOI":"10.1038\/ncb3438","article-title":"Engulfed cadherin fingers are polarized junctional structures between collectively migrating endothelial cells","volume":"18","author":"Hayer","year":"2016","journal-title":"Nat. Cell Biol."},{"key":"2023053109142731500_JCS260827C34","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1083\/jcb.141.1.85","article-title":"Dynamin-mediated internalization of caveolae","volume":"141","author":"Henley","year":"1998","journal-title":"J. Cell Biol."},{"key":"2023053109142731500_JCS260827C35","doi-asserted-by":"publisher","first-page":"1739","DOI":"10.1242\/jcs.078014","article-title":"Cdc42-interacting protein 4 is a Src substrate that regulates invadopodia and invasiveness of breast tumors by promoting MT1-MMP endocytosis","volume":"124","author":"Hu","year":"2011","journal-title":"J. Cell Sci."},{"key":"2023053109142731500_JCS260827C36","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1083\/jcb.200205115","article-title":"A novel role for p120 catenin in E-cadherin function","volume":"159","author":"Ireton","year":"2002","journal-title":"J. Cell Biol."},{"key":"2023053109142731500_JCS260827C37","doi-asserted-by":"publisher","first-page":"7624","DOI":"10.3390\/ijms21207624","article-title":"Role of cadherins in cancer-a review","volume":"21","author":"Kaszak","year":"2020","journal-title":"Int. J. Mol. Sci."},{"key":"2023053109142731500_JCS260827C38","doi-asserted-by":"publisher","first-page":"5840","DOI":"10.1038\/onc.2017.171","article-title":"Cadherin composition and multicellular aggregate invasion in organotypic models of epithelial ovarian cancer intraperitoneal metastasis","volume":"36","author":"Klymenko","year":"2017","journal-title":"Oncogene"},{"key":"2023053109142731500_JCS260827C39","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1007\/978-94-007-4186-7_9","article-title":"Adherens junction turnover: regulating adhesion through cadherin endocytosis, degradation, and recycling","volume":"60","author":"Kowalczyk","year":"2012","journal-title":"Subcell. Biochem."},{"key":"2023053109142731500_JCS260827C40","doi-asserted-by":"publisher","first-page":"e202207020","DOI":"10.1083\/jcb.202207020","article-title":"ARHGAP17 regulates the spatiotemporal activity of Cdc42 at invadopodia","volume":"222","author":"Kreider-Letterman","year":"2023","journal-title":"J. Cell Biol."},{"key":"2023053109142731500_JCS260827C41","doi-asserted-by":"publisher","first-page":"952","DOI":"10.1038\/onc.2015.155","article-title":"LPP inhibits collective cell migration during lung cancer dissemination","volume":"35","author":"Kuriyama","year":"2016","journal-title":"Oncogene"},{"key":"2023053109142731500_JCS260827C42","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1083\/jcb.146.999.219","article-title":"Recycling of E-cadherin: A potential mechanism for regulating cadherin dynamics","volume":"146","author":"Le","year":"1999","journal-title":"J. Cell Biol."},{"key":"2023053109142731500_JCS260827C43","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/j.bbrc.2021.07.041","article-title":"Dynamin 2 and BAR domain protein pacsin 2 cooperatively regulate formation and maturation of podosomes","volume":"571","author":"Li","year":"2021","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"2023053109142731500_JCS260827C44","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1016\/S1535-6108(03)00304-0","article-title":"Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of \u03b2-catenin, and enhanced tumor cell invasion","volume":"4","author":"Lu","year":"2003","journal-title":"Cancer Cell"},{"key":"2023053109142731500_JCS260827C45","doi-asserted-by":"publisher","first-page":"873","DOI":"10.1242\/jcs.01634","article-title":"Cadherin switching: essential for behavioral but not morphological changes during an epithelium-to-mesenchyme transition","volume":"118","author":"Maeda","year":"2005","journal-title":"J. Cell Sci."},{"key":"2023053109142731500_JCS260827C46","doi-asserted-by":"publisher","first-page":"2610","DOI":"10.1038\/s41467-021-22873-y","article-title":"A junctional PACSIN2\/EHD4\/MICAL-L1 complex coordinates VE-cadherin trafficking for endothelial migration and angiogenesis","volume":"12","author":"Malinova","year":"2021","journal-title":"Nat. Commun."},{"key":"2023053109142731500_JCS260827C47","doi-asserted-by":"publisher","first-page":"73","DOI":"10.4161\/cc.10.1.14243","article-title":"PACSIN 2 represses cellular migration through direct association with cyclin D1 but not its alternate splice form cyclin D1b","volume":"10","author":"Meng","year":"2011","journal-title":"Cell Cycle"},{"key":"2023053109142731500_JCS260827C48","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1186\/s12885-018-4358-x","article-title":"Small cell and non small cell lung cancer form metastasis on cellular 4D lung model","volume":"18","author":"Mishra","year":"2018","journal-title":"BMC Cancer"},{"key":"2023053109142731500_JCS260827C49","doi-asserted-by":"publisher","first-page":"11540","DOI":"10.1074\/jbc.M608351200","article-title":"Increased internalization of p120-uncoupled E-cadherin and a requirement for a dileucine motif in the cytoplasmic domain for endocytosis of the protein","volume":"282","author":"Miyashita","year":"2007","journal-title":"J. Biol. Chem."},{"key":"2023053109142731500_JCS260827C50","doi-asserted-by":"publisher","first-page":"4511","DOI":"10.1242\/jcs.113.24.4511","article-title":"All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis","volume":"113","author":"Modregger","year":"2000","journal-title":"J. Cell Sci."},{"key":"2023053109142731500_JCS260827C51","doi-asserted-by":"publisher","first-page":"2220","DOI":"10.1074\/jbc.M406906200","article-title":"Rab13 mediates the continuous endocytic recycling of occludin to the cell surface","volume":"280","author":"Morimoto","year":"2005","journal-title":"J. Biol. Chem."},{"key":"2023053109142731500_JCS260827C52","doi-asserted-by":"publisher","first-page":"939","DOI":"10.1186\/s12885-018-4845-0","article-title":"N-cadherin in cancer metastasis, its emerging role in haematological malignancies and potential as a therapeutic target in cancer","volume":"18","author":"Mrozik","year":"2018","journal-title":"BMC Cancer"},{"key":"2023053109142731500_JCS260827C53","doi-asserted-by":"publisher","first-page":"1093","DOI":"10.1242\/jcs.183699","article-title":"The mechanical regulation of integrin-cadherin crosstalk organizes cells, signaling and forces","volume":"129","author":"Mui","year":"2016","journal-title":"J. Cell Sci."},{"key":"2023053109142731500_JCS260827C54","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/j.cell.2016.06.028","article-title":"Emt: 2016","volume":"166","author":"Nieto","year":"2016","journal-title":"Cell"},{"key":"2023053109142731500_JCS260827C55","doi-asserted-by":"publisher","first-page":"1137","DOI":"10.1083\/jcb.201008173","article-title":"Evolution: structural and functional diversity of cadherin at the adherens junction","volume":"193","author":"Oda","year":"2011","journal-title":"J. Cell Biol."},{"key":"2023053109142731500_JCS260827C56","doi-asserted-by":"publisher","first-page":"1589","DOI":"10.1038\/ncomms2560","article-title":"N-cadherin regulates spatially polarized signals through distinct p120ctn and \u03b2-catenin-dependent signalling pathways","volume":"4","author":"Ouyang","year":"2013","journal-title":"Nat. Commun."},{"key":"2023053109142731500_JCS260827C57","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1002\/1878-0261.12019","article-title":"Modes of invasion during tumour dissemination","volume":"11","author":"Pandya","year":"2017","journal-title":"Mol. Oncol."},{"key":"2023053109142731500_JCS260827C58","doi-asserted-by":"publisher","first-page":"21050","DOI":"10.1074\/jbc.M300082200","article-title":"Characterization of E-cadherin endocytosis in isolated MCF-7 and Chinese hamster ovary cells. The initial fate of unbound E-cadherin","volume":"278","author":"Paterson","year":"2003","journal-title":"J. Biol. Chem."},{"key":"2023053109142731500_JCS260827C59","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1126\/science.1092586","article-title":"BAR domains as sensors of membrane curvature: the amphiphysin BAR structure","volume":"303","author":"Peter","year":"2004","journal-title":"Science"},{"key":"2023053109142731500_JCS260827C60","doi-asserted-by":"publisher","first-page":"8347","DOI":"10.1158\/0008-5472.CAN-09-4149","article-title":"Cdc42-interacting protein 4 promotes breast cancer cell invasion and formation of invadopodia through activation of N-WASp","volume":"70","author":"Pichot","year":"2010","journal-title":"Cancer Res."},{"key":"2023053109142731500_JCS260827C61","doi-asserted-by":"publisher","first-page":"10688","DOI":"10.1523\/JNEUROSCI.5132-13.2014","article-title":"The BAR domain protein PICK1 controls vesicle number and size in adrenal chromaffin cells","volume":"34","author":"Pinheiro","year":"2014","journal-title":"J. Neurosci."},{"key":"2023053109142731500_JCS260827C62","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1083\/jcb.201505105","article-title":"P-cadherin promotes collective cell migration via a Cdc42-mediated increase in mechanical forces","volume":"212","author":"Plutoni","year":"2016","journal-title":"J. Cell Biol."},{"key":"2023053109142731500_JCS260827C63","doi-asserted-by":"publisher","first-page":"1047","DOI":"10.1083\/jcb.148.5.1047","article-title":"Syndapin isoforms participate in receptor-mediated endocytosis and actin organization","volume":"148","author":"Qualmann","year":"2000","journal-title":"J. Cell Biol."},{"key":"2023053109142731500_JCS260827C64","doi-asserted-by":"publisher","first-page":"3501","DOI":"10.1038\/emboj.2011.266","article-title":"Let's go bananas: revisiting the endocytic BAR code","volume":"30","author":"Qualmann","year":"2011","journal-title":"EMBO J."},{"key":"2023053109142731500_JCS260827C65","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1038\/nrm3431","article-title":"A bigger picture: classical cadherins and the dynamic actin cytoskeleton","volume":"13","author":"Ratheesh","year":"2012","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023053109142731500_JCS260827C66","doi-asserted-by":"publisher","first-page":"14923","DOI":"10.1038\/ncomms14923","article-title":"Anisotropic forces from spatially constrained focal adhesions mediate contact guidance directed cell migration","volume":"8","author":"Ray","year":"2017","journal-title":"Nat. Commun."},{"key":"2023053109142731500_JCS260827C67","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1016\/j.bbamcr.2006.09.019","article-title":"p120-catenin: past and present","volume":"1773","author":"Reynolds","year":"2007","journal-title":"Biochim. Biophys. Acta"},{"key":"2023053109142731500_JCS260827C68","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1146\/annurev.cellbio.042308.113231","article-title":"Collective cell migration","volume":"25","author":"R\u00f8rth","year":"2009","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"2023053109142731500_JCS260827C69","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1161\/CIRCRESAHA.108.175307","article-title":"Homotypic and endothelial cell adhesions via N-cadherin determine polarity and regulate migration of vascular smooth muscle cells","volume":"103","author":"Sabatini","year":"2008","journal-title":"Circ. Res."},{"key":"2023053109142731500_JCS260827C70","doi-asserted-by":"publisher","first-page":"91","DOI":"10.3390\/membranes2010091","article-title":"The BAR domain superfamily proteins from subcellular structures to human diseases","volume":"2","author":"Safari","year":"2012","journal-title":"Membranes (Basel)"},{"key":"2023053109142731500_JCS260827C71","doi-asserted-by":"publisher","first-page":"e52401","DOI":"10.1371\/journal.pone.0052401","article-title":"Bin2 is a membrane sculpting N-BAR protein that influences leucocyte podosomes, motility and phagocytosis","volume":"7","author":"S\u00e1nchez-Barrena","year":"2012","journal-title":"PLoS ONE"},{"key":"2023053109142731500_JCS260827C72","doi-asserted-by":"publisher","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: an open-source platform for biological-image analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. Methods"},{"key":"2023053109142731500_JCS260827C73","doi-asserted-by":"publisher","first-page":"671","DOI":"10.1038\/nmeth.2089","article-title":"NIH Image to ImageJ: 25 years of image analysis","volume":"9","author":"Schneider","year":"2012","journal-title":"Nat. Methods"},{"key":"2023053109142731500_JCS260827C74","doi-asserted-by":"publisher","first-page":"2032","DOI":"10.1242\/jcs.086264","article-title":"Essential role of PACSIN2\/syndapin-II in caveolae membrane sculpting","volume":"124","author":"Senju","year":"2011","journal-title":"J. Cell Sci."},{"key":"2023053109142731500_JCS260827C75","doi-asserted-by":"publisher","first-page":"690","DOI":"10.1038\/s41586-021-04210-x","article-title":"Collective durotaxis along a self-generated stiffness gradient in vivo","volume":"600","author":"Shellard","year":"2021","journal-title":"Nature"},{"key":"2023053109142731500_JCS260827C76","doi-asserted-by":"publisher","first-page":"3661","DOI":"10.1242\/jcs.103861","article-title":"N-cadherin-mediated cell-cell adhesion promotes cell migration in a three-dimensional matrix","volume":"125","author":"Shih","year":"2012","journal-title":"J. Cell Sci."},{"key":"2023053109142731500_JCS260827C77","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.isci.2018.08.014","article-title":"Caveolin-1 promotes early neuronal maturation via caveolae-independent trafficking of N-cadherin and L1","volume":"7","author":"Shikanai","year":"2018","journal-title":"iScience"},{"key":"2023053109142731500_JCS260827C78","doi-asserted-by":"publisher","first-page":"130081","DOI":"10.1098\/rsob.130081","article-title":"Drosophila F-BAR protein Syndapin contributes to coupling the plasma membrane and contractile ring in cytokinesis","volume":"3","author":"Takeda","year":"2013","journal-title":"Open Biol."},{"key":"2023053109142731500_JCS260827C79","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1038\/9004","article-title":"Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis","volume":"1","author":"Takei","year":"1999","journal-title":"Nat. Cell Biol."},{"key":"2023053109142731500_JCS260827C80","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1016\/j.devcel.2010.06.012","article-title":"Collective chemotaxis requires contact-dependent cell polarity","volume":"19","author":"Theveneau","year":"2010","journal-title":"Dev. Cell"},{"key":"2023053109142731500_JCS260827C81","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1038\/nrm1835","article-title":"Complex networks orchestrate epithelial-mesenchymal transitions","volume":"7","author":"Thiery","year":"2006","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023053109142731500_JCS260827C82","doi-asserted-by":"publisher","first-page":"2722","DOI":"10.1038\/emboj.2013.212","article-title":"Endophilin, lamellipodin, and mena cooperate to regulate F-actin-dependent EGF-receptor endocytosis","volume":"32","author":"Vehlow","year":"2013","journal-title":"EMBO J."},{"key":"2023053109142731500_JCS260827C83","doi-asserted-by":"publisher","first-page":"1529","DOI":"10.1091\/mbc.e10-09-0785","article-title":"A direct interaction between the large GTPase dynamin-2 and FAK regulates focal adhesion dynamics in response to active Src","volume":"22","author":"Wang","year":"2011","journal-title":"Mol. Biol. Cell"},{"key":"2023053109142731500_JCS260827C84","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1111\/pin.12391","article-title":"Collective invasion of cancer: perspectives from pathology and development","volume":"66","author":"Wang","year":"2016","journal-title":"Pathol. Int."},{"key":"2023053109142731500_JCS260827C85","doi-asserted-by":"publisher","first-page":"727","DOI":"10.1242\/jcs.000455","article-title":"Cadherin switching","volume":"121","author":"Wheelock","year":"2008","journal-title":"J. Cell Sci."},{"key":"2023053109142731500_JCS260827C86","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1042\/bj20021962","article-title":"MIM-B, a putative metastasis suppressor protein, binds to actin and to protein tyrosine phosphatase delta","volume":"371","author":"Woodings","year":"2003","journal-title":"Biochem. J."},{"key":"2023053109142731500_JCS260827C87","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1083\/jcb.200306001","article-title":"Cellular levels of p120 catenin function as a set point for cadherin expression levels in microvascular endothelial cells","volume":"163","author":"Xiao","year":"2003","journal-title":"J. Cell Biol."},{"key":"2023053109142731500_JCS260827C88","doi-asserted-by":"publisher","first-page":"19199","DOI":"10.1074\/jbc.M211746200","article-title":"Mechanisms of VE-cadherin processing and degradation in microvascular endothelial cells","volume":"278","author":"Xiao","year":"2003","journal-title":"J. Biol. Chem."},{"key":"2023053109142731500_JCS260827C89","doi-asserted-by":"publisher","first-page":"1169","DOI":"10.1101\/gad.14.10.1169","article-title":"Cadherin superfamily genes: functions, genomic organization, and neurologic diversity","volume":"14","author":"Yagi","year":"2000","journal-title":"Genes Dev."},{"key":"2023053109142731500_JCS260827C90","doi-asserted-by":"publisher","first-page":"738","DOI":"10.1038\/s41580-019-0172-9","article-title":"Mechanisms of 3D cell migration","volume":"20","author":"Yamada","year":"2019","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023053109142731500_JCS260827C91","doi-asserted-by":"publisher","first-page":"1930","DOI":"10.1016\/j.juro.2010.12.027","article-title":"Requirement for FBP17 in invadopodia formation by invasive bladder tumor cells","volume":"185","author":"Yamamoto","year":"2011","journal-title":"J. Urol."},{"key":"2023053109142731500_JCS260827C92","first-page":"5301","article-title":"An emerging tumor invasion mechanism about the collective cell migration","volume":"11","author":"Yang","year":"2019","journal-title":"Am. J. Transl. Res."},{"key":"2023053109142731500_JCS260827C93","doi-asserted-by":"publisher","first-page":"409","DOI":"10.1016\/j.bbrc.2016.10.063","article-title":"Dynamin2 GTPase contributes to invadopodia formation in invasive bladder cancer cells","volume":"480","author":"Zhang","year":"2016","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"2023053109142731500_JCS260827C94","doi-asserted-by":"publisher","first-page":"696072","DOI":"10.3389\/fmolb.2021.696072","article-title":"Decreased expression of PACSIN1 in brain glioma samples predicts poor prognosis","volume":"8","author":"Zimu","year":"2021","journal-title":"Front. Mol. Biosci."},{"key":"2023053109142731500_JCS260827C95","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.bpj.2021.12.006","article-title":"Disentangling cadherin-mediated cell-cell interactions in collective cancer cell migration","volume":"1","author":"Zisis","year":"2022","journal-title":"Biophys. J."}],"container-title":["Journal of Cell Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.biologists.com\/jcs\/article-pdf\/doi\/10.1242\/jcs.260827\/2822990\/jcs260827.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/jcs\/article-pdf\/doi\/10.1242\/jcs.260827\/2870836\/jcs260827.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/jcs\/article-pdf\/doi\/10.1242\/jcs.260827\/2870836\/jcs260827.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,31]],"date-time":"2023-05-31T05:20:04Z","timestamp":1685510404000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jcs\/article\/136\/10\/jcs260827\/310877\/Pacsin-2-dependent-N-cadherin-internalization"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,15]]},"references-count":95,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2023,5,15]]}},"URL":"https:\/\/doi.org\/10.1242\/jcs.260827","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2022.08.08.502718","asserted-by":"object"}]},"ISSN":["0021-9533","1477-9137"],"issn-type":[{"value":"0021-9533","type":"print"},{"value":"1477-9137","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,15]]},"article-number":"jcs260827"}}