{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,11]],"date-time":"2026-02-11T12:49:00Z","timestamp":1770814140643,"version":"3.50.1"},"reference-count":50,"publisher":"The Company of Biologists","issue":"3","license":[{"start":{"date-parts":[[2026,2,1]],"date-time":"2026-02-01T00:00:00Z","timestamp":1769904000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.biologists.com\/user-licence-1-2\/"}],"funder":[{"DOI":"10.13039\/501100004794","name":"Centre National de la Recherche Scientifique","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100004794","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Universit\u00e9 Paris Cit\u00e9"},{"DOI":"10.13039\/501100001665","name":"L'Agence nationale de la recherche","doi-asserted-by":"crossref","award":["ANR-18-IDEX-0001"],"award-info":[{"award-number":["ANR-18-IDEX-0001"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Minist\u00e8re de l'Enseignement Sup\u00e9rieur de la Recherche Scientifique et des Technologies de l'Information et de la Communication"},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"crossref","award":["RGPIN-2020-06367"],"award-info":[{"award-number":["RGPIN-2020-06367"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,2,1]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>Morphogenesis is orchestrated through coordinated cell movements, including cell intercalation, which drives extensive changes in cell shape and position. This process requires precise regulation of interactions between adherens junctions (AJs) and the cortical actin network to generate the necessary mechanical forces. Although the Myosin molecular motor II plays a central role in generating morphogenetic forces, it is dispensable for processes such as dorsal branch morphogenesis in the Drosophila tracheal system, where coordinated cell migration and three-dimensional intercalation rely on alternative, yet poorly characterised mechanisms of force generation. Here, we show that Vinculin and Ajuba LIM protein, two key regulators of mechano-transduction and cell adhesion, do not localise to AJs of dorsal branches, while the cytoskeletal adaptor Girdin does. We demonstrate that the function of Girdin relies on AJ components \u03b1-Catenin and E-Cadherin, and is specifically required in tracheal cells to ensure the proper pace of cell intercalation. In addition, Girdin contributes to the actin network enrichment at AJs. Its role as an integral AJ component is further elucidated through the development of a novel genetic tool that enables in vivo cell-specific actin depolymerisation.<\/jats:p>","DOI":"10.1242\/dev.205073","type":"journal-article","created":{"date-parts":[[2026,1,15]],"date-time":"2026-01-15T09:55:54Z","timestamp":1768470954000},"source":"Crossref","is-referenced-by-count":0,"title":["Girdin controls the pace of 3D tracheal cell intercalation by coupling adherens junctions to the actin cytoskeleton in\n                    <i>Drosophila<\/i>"],"prefix":"10.1242","volume":"153","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8654-0539","authenticated-orcid":false,"given":"Sandra","family":"Carvalho","sequence":"first","affiliation":[{"name":"Universit\u00e9 Paris Cit\u00e9, CNRS, Institut Jacques Monod 1 , Paris 75205 Cedex 13,","place":["France"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9785-4376","authenticated-orcid":false,"given":"Patrick","family":"Laprise","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Laval 2 D\u00e9partement de biologie mol\u00e9culaire, de biochimie m\u00e9dicale et de pathologie, Facult\u00e9 de m\u00e9decine , , Qu\u00e9bec, QC G1V0A6 ,","place":["Canada"]},{"name":"PROTEO et Centre de Recherche sur le Cancer de l'Universit\u00e9 Laval 3 , Qu\u00e9bec, G1J 0J9 ,","place":["Canada"]},{"name":"Axe Oncologie du Centre de Recherche du Centre Hospitalier Universitaire de Qu\u00e9bec-UL 4 , 2260 Henri-Bourassa, Qu\u00e9bec, QC G1J 5B3 ,","place":["Canada"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7216-1944","authenticated-orcid":false,"given":"Antoine","family":"Guichet","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris Cit\u00e9, CNRS, Institut Jacques Monod 1 , Paris 75205 Cedex 13,","place":["France"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0916-5050","authenticated-orcid":false,"given":"V\u00e9ronique","family":"Brodu","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris Cit\u00e9, CNRS, Institut Jacques Monod 1 , Paris 75205 Cedex 13,","place":["France"]}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","published-online":{"date-parts":[[2026,2,11]]},"reference":[{"key":"2026021104071836500_DEV205073C1","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1016\/S0014-5793(97)00901-0","article-title":"Vinculin gene is non-essential in Drosophila melanogaster","volume":"413","author":"Alatortsev","year":"1997","journal-title":"FEBS Lett."},{"key":"2026021104071836500_DEV205073C2","doi-asserted-by":"publisher","first-page":"715","DOI":"10.1083\/jcb.114.4.715","article-title":"Vinculin is essential for muscle function in the nematode","volume":"114","author":"Barstead","year":"1991","journal-title":"J. Cell Biol."},{"key":"2026021104071836500_DEV205073C3","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1242\/dev.118.2.401","article-title":"Targeted gene expression as a means of altering cell fates and generating dominant phenotypes","volume":"118","author":"Brand","year":"1993","journal-title":"Development"},{"key":"2026021104071836500_DEV205073C4","doi-asserted-by":"publisher","first-page":"1817","DOI":"10.1101\/gad.375706","article-title":"The RhoGAP crossveinless-c links trachealess and EGFR signaling to cell shape remodeling in Drosophila tracheal invagination","volume":"20","author":"Brodu","year":"2006","journal-title":"Genes Dev."},{"key":"2026021104071836500_DEV205073C5","doi-asserted-by":"publisher","first-page":"885","DOI":"10.1016\/j.devcel.2004.10.016","article-title":"EGF receptor signaling regulates pulses of cell delamination from the Drosophila ectoderm","volume":"7","author":"Brodu","year":"2004","journal-title":"Dev. Cell"},{"key":"2026021104071836500_DEV205073C6","doi-asserted-by":"publisher","first-page":"790","DOI":"10.1016\/j.devcel.2010.03.015","article-title":"A developmentally regulated two-step process generates a noncentrosomal microtubule network in Drosophila tracheal cells","volume":"18","author":"Brodu","year":"2010","journal-title":"Dev. Cell"},{"key":"2026021104071836500_DEV205073C7","doi-asserted-by":"publisher","first-page":"822","DOI":"10.1002\/cm.20226","article-title":"Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin","volume":"64","author":"Burkel","year":"2007","journal-title":"Cell Motil. Cytoskelet."},{"key":"2026021104071836500_DEV205073C8","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-662-02454-6","volume-title":"The Embryonic Development of Drosophila melanogaster","author":"Campos-Ortega","year":"1985"},{"key":"2026021104071836500_DEV205073C9","doi-asserted-by":"publisher","first-page":"252","DOI":"10.1038\/s41580-023-00688-7","article-title":"Adherens junctions as molecular regulators of emergent tissue mechanics","volume":"25","author":"Camp\u00e0s","year":"2024","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2026021104071836500_DEV205073C10","doi-asserted-by":"publisher","first-page":"1727","DOI":"10.1016\/j.cub.2008.10.062","article-title":"Tip-cell migration controls stalk-cell intercalation during drosophila tracheal tube elongation","volume":"18","author":"Caussinus","year":"2008","journal-title":"Curr. Biol."},{"key":"2026021104071836500_DEV205073C11","doi-asserted-by":"publisher","first-page":"751","DOI":"10.1038\/nature06953","article-title":"A two-tiered mechanism for stabilization and immobilization of E-cadherin","volume":"453","author":"Cavey","year":"2008","journal-title":"Nature"},{"key":"2026021104071836500_DEV205073C12","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1016\/j.devcel.2005.08.001","article-title":"Akt\/PKB regulates actin organization and cell motility via Girdin\/APE","volume":"9","author":"Enomoto","year":"2005","journal-title":"Dev. Cell"},{"key":"2026021104071836500_DEV205073C13","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1196\/annals.1377.016","article-title":"Girdin, a novel actin-binding protein, and its family of proteins possess versatile functions in the Akt and Wnt signaling pathways","volume":"1086","author":"Enomoto","year":"2006","journal-title":"Ann. N Y Acad. Sci."},{"key":"2026021104071836500_DEV205073C14","doi-asserted-by":"publisher","first-page":"981","DOI":"10.1016\/S0092-8674(00)00200-2","article-title":"Gradient Formation of the TGF-\u03b2 Homolog Dpp","volume":"103","author":"Entchev","year":"2000","journal-title":"Cell"},{"key":"2026021104071836500_DEV205073C15","doi-asserted-by":"publisher","first-page":"4819","DOI":"10.1242\/dev.02056","article-title":"Rho1 regulates Drosophila adherens junctions independently of p120ctn","volume":"132","author":"Fox","year":"2005","journal-title":"Development"},{"key":"2026021104071836500_DEV205073C16","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":"2026021104071836500_DEV205073C17","doi-asserted-by":"publisher","first-page":"a029199","DOI":"10.1101\/cshperspect.a029199","article-title":"Tuning collective cell migration by cell\u2013cell junction regulation","volume":"9","author":"Friedl","year":"2017","journal-title":"Cold Spring Harbor Perspect. Biol."},{"key":"2026021104071836500_DEV205073C18","doi-asserted-by":"publisher","first-page":"e0182278","DOI":"10.1371\/journal.pone.0182278","article-title":"Zygotic vinculin is not essential for embryonic development in zebrafish","volume":"12","author":"Han","year":"2017","journal-title":"PLoS ONE"},{"key":"2026021104071836500_DEV205073C19","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1038\/nmeth.4257","article-title":"DeActs: genetically encoded tools for perturbing the actin cytoskeleton in single cells","volume":"14","author":"Harterink","year":"2017","journal-title":"Nat. Methods"},{"key":"2026021104071836500_DEV205073C20","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1534\/genetics.117.300167","article-title":"Development and Function of the Drosophila Tracheal System","volume":"209","author":"Hayashi","year":"2018","journal-title":"Genetics"},{"key":"2026021104071836500_DEV205073C21","doi-asserted-by":"publisher","first-page":"1777","DOI":"10.1242\/dev.122002","article-title":"Girdin-mediated interactions between cadherin and the actin cytoskeleton are required for epithelial morphogenesis in Drosophila","volume":"142","author":"Houssin","year":"2015","journal-title":"Development"},{"key":"2026021104071836500_DEV205073C22","doi-asserted-by":"publisher","first-page":"1224","DOI":"10.1016\/j.cub.2006.04.048","article-title":"Polychaetoid\/ZO-1 is required for cell specification and rearrangement during Drosophila tracheal morphogenesis","volume":"16","author":"Jung","year":"2006","journal-title":"Curr. Biol."},{"key":"2026021104071836500_DEV205073C23","doi-asserted-by":"publisher","first-page":"5021","DOI":"10.1038\/s41467-018-07448-8","article-title":"Distinct contributions of tensile and shear stress on E-cadherin levels during morphogenesis","volume":"9","author":"Kale","year":"2018","journal-title":"Nat. Commun."},{"key":"2026021104071836500_DEV205073C24","doi-asserted-by":"publisher","first-page":"11141","DOI":"10.1038\/ncomms11141","article-title":"Microtubule-dependent balanced cell contraction and luminal-matrix modification accelerate epithelial tube fusion","volume":"7","author":"Kato","year":"2016","journal-title":"Nat. Commun."},{"key":"2026021104071836500_DEV205073C25","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1038\/nature11792","article-title":"Mitotic cell rounding accelerates epithelial invagination","volume":"494","author":"Kondo","year":"2013","journal-title":"Nature"},{"key":"2026021104071836500_DEV205073C26","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1242\/dev.113472","article-title":"Microtubule-dependent apical restriction of recycling endosomes sustains adherens junctions during morphogenesis of the Drosophila tracheal system","volume":"142","author":"Le Droguen","year":"2015","journal-title":"Development"},{"key":"2026021104071836500_DEV205073C27","doi-asserted-by":"publisher","first-page":"1107","DOI":"10.1083\/jcb.201001149","article-title":"Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner","volume":"189","author":"le Duc","year":"2010","journal-title":"J. Cell Biol."},{"key":"2026021104071836500_DEV205073C28","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1016\/j.devcel.2019.07.007","article-title":"Sidekick is a key component of tricellular adherens junctions that acts to resolve cell rearrangements","volume":"50","author":"Letizia","year":"2019","journal-title":"Dev. Cell"},{"key":"2026021104071836500_DEV205073C29","doi-asserted-by":"publisher","first-page":"4354","DOI":"10.1242\/jcs.189878","article-title":"Drosophila vinculin is more harmful when hyperactive than absent, and can circumvent integrin to form adhesion complexes","volume":"129","author":"Maartens","year":"2016","journal-title":"J. Cell Sci."},{"key":"2026021104071836500_DEV205073C30","doi-asserted-by":"publisher","first-page":"877","DOI":"10.1016\/j.devcel.2009.04.010","article-title":"Apical secretion in epithelial tubes of the Drosophila embryo is directed by the Formin-family protein diaphanous","volume":"16","author":"Massarwa","year":"2009","journal-title":"Dev. Cell"},{"key":"2026021104071836500_DEV205073C31","doi-asserted-by":"publisher","first-page":"dev172056","DOI":"10.1242\/dev.172056","article-title":"Cell interactions in collective cell migration","volume":"146","author":"Mishra","year":"2019","journal-title":"Development"},{"key":"2026021104071836500_DEV205073C32","doi-asserted-by":"publisher","first-page":"4375","DOI":"10.1242\/dev.126.19.4375","article-title":"Directionality of wingless protein transport influences epidermal patterning in the Drosophila embryo","volume":"126","author":"Moline","year":"1999","journal-title":"Development"},{"key":"2026021104071836500_DEV205073C33","doi-asserted-by":"publisher","first-page":"2961","DOI":"10.1242\/dev.148940","article-title":"Myosin II is not required for Drosophila tracheal branch elongation and cell intercalation","volume":"144","author":"Ochoa-Espinosa","year":"2017","journal-title":"Development"},{"key":"2026021104071836500_DEV205073C34","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1016\/bs.ctdb.2019.11.014","article-title":"Cellular, molecular, and biophysical control of epithelial cell intercalation","volume":"136","author":"Par\u00e9","year":"2020","journal-title":"Curr. Top. Dev. Biol."},{"key":"2026021104071836500_DEV205073C35","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.devcel.2018.09.014","article-title":"Mechanical force-driven adherens junction remodeling and epithelial dynamics","volume":"47","author":"Pinheiro","year":"2018","journal-title":"Dev. Cell"},{"key":"2026021104071836500_DEV205073C36","doi-asserted-by":"publisher","first-page":"1110","DOI":"10.1038\/nature09566","article-title":"Planar polarized actomyosin contractile flows control epithelial junction remodelling","volume":"468","author":"Rauzi","year":"2010","journal-title":"Nature"},{"key":"2026021104071836500_DEV205073C37","doi-asserted-by":"publisher","first-page":"3715","DOI":"10.1083\/jcb.201801171","article-title":"The force-sensitive protein Ajuba regulates cell adhesion during epithelial morphogenesis","volume":"217","author":"Razzell","year":"2018","journal-title":"J. Cell Biol."},{"key":"2026021104071836500_DEV205073C38","doi-asserted-by":"publisher","first-page":"2197","DOI":"10.1016\/j.cub.2004.11.056","article-title":"Genetic control of cell intercalation during tracheal morphogenesis in Drosophila","volume":"14","author":"Ribeiro","year":"2004","journal-title":"Curr. Biol."},{"key":"2026021104071836500_DEV205073C39","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1242\/jcs.096644","article-title":"Mutational analysis supports a core role for Drosophila \u03b1-Catenin in adherens junction function","volume":"125","author":"Sarpal","year":"2012","journal-title":"J. Cell Sci."},{"key":"2026021104071836500_DEV205073C40","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":"2026021104071836500_DEV205073C41","doi-asserted-by":"publisher","first-page":"964","DOI":"10.1038\/ncb1756","article-title":"Modulation of intracellular trafficking regulates cell intercalation in the Drosophila trachea","volume":"10","author":"Shaye","year":"2008","journal-title":"Nat. Cell Biol."},{"key":"2026021104071836500_DEV205073C42","doi-asserted-by":"publisher","first-page":"e202108091","DOI":"10.1083\/jcb.202108091","article-title":"The \u03b1-Catenin mechanosensing M region is required for cell adhesion during tissue morphogenesis","volume":"222","author":"Sheppard","year":"2023","journal-title":"J. Cell Biol."},{"key":"2026021104071836500_DEV205073C43","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1046\/j.1440-169X.1996.00012.x","article-title":"A nuclear GFP\/\u03b2-galactosidase fusion protein as a marker for morphogenesis in living Drosophila","volume":"38","author":"Shiga","year":"1996","journal-title":"Dev. Growth Differ."},{"key":"2026021104071836500_DEV205073C44","doi-asserted-by":"publisher","first-page":"672","DOI":"10.1101\/gad.10.6.672","article-title":"Shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia","volume":"10","author":"Tepass","year":"1996","journal-title":"Genes Dev."},{"key":"2026021104071836500_DEV205073C45","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1016\/j.devcel.2005.07.012","article-title":"A transient luminal chitinous matrix is required to model epithelial tube diameter in the Drosophila trachea","volume":"9","author":"Tonning","year":"2005","journal-title":"Dev. Cell"},{"key":"2026021104071836500_DEV205073C46","doi-asserted-by":"publisher","first-page":"180","DOI":"10.1016\/j.cub.2005.11.074","article-title":"Septate-junction-dependent luminal deposition of chitin deacetylases restricts tube elongation in the drosophila trachea","volume":"16","author":"Wang","year":"2006","journal-title":"Curr. Biol."},{"key":"2026021104071836500_DEV205073C47","doi-asserted-by":"publisher","first-page":"3643","DOI":"10.1111\/cas.13795","article-title":"Girdin\/GIV regulates collective cancer cell migration by controlling cell adhesion and cytoskeletal organization","volume":"109","author":"Wang","year":"2018","journal-title":"Cancer Sci."},{"key":"2026021104071836500_DEV205073C48","doi-asserted-by":"publisher","first-page":"2098","DOI":"10.15252\/embj.201488289","article-title":"Regulation of cargo-selective endocytosis by dynamin 2 GTP ase-activating protein girdin","volume":"33","author":"Weng","year":"2014","journal-title":"EMBO J."},{"key":"2026021104071836500_DEV205073C49","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1242\/dev.125.2.327","article-title":"Vinculin knockout results in heart and brain defects during embryonic development","volume":"125","author":"Xu","year":"1998","journal-title":"Development"},{"key":"2026021104071836500_DEV205073C50","doi-asserted-by":"publisher","first-page":"4525","DOI":"10.1038\/ncomms5525","article-title":"Force-dependent conformational switch of \u03b1-catenin controls vinculin binding","volume":"5","author":"Yao","year":"2014","journal-title":"Nat. Commun."}],"container-title":["Development"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.205073\/3680975\/dev205073.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.205073\/3684171\/dev205073.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.205073\/3684171\/dev205073.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,2,11]],"date-time":"2026-02-11T09:07:29Z","timestamp":1770800849000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/dev\/article\/153\/3\/dev205073\/370627\/Girdin-controls-the-pace-of-3D-tracheal-cell"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,2,1]]},"references-count":50,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2026,2,1]]}},"URL":"https:\/\/doi.org\/10.1242\/dev.205073","relation":{},"ISSN":["0950-1991","1477-9129"],"issn-type":[{"value":"0950-1991","type":"print"},{"value":"1477-9129","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,2,1]]},"article-number":"dev205073"}}