{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T09:08:20Z","timestamp":1791364100505,"version":"4.3.1"},"reference-count":86,"publisher":"Rockefeller University Press","issue":"6","content-domain":{"domain":["rupress.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2015,9,14]]},"abstract":"<jats:p>Invasive migration in 3D extracellular matrix (ECM) is crucial to cancer metastasis, yet little is known of the molecular mechanisms that drive reorganization of the cytoskeleton as cancer cells disseminate in vivo. 2D Rac-driven lamellipodial migration is well understood, but how these features apply to 3D migration is not clear. We find that lamellipodia-like protrusions and retrograde actin flow are indeed observed in cells moving in 3D ECM. However, Rab-coupling protein (RCP)-driven endocytic recycling of \u03b15\u03b21 integrin enhances invasive migration of cancer cells into fibronectin-rich 3D ECM, driven by RhoA and filopodial spike-based protrusions, not lamellipodia. Furthermore, we show that actin spike protrusions are Arp2\/3-independent. Dynamic actin spike assembly in cells invading in vitro and in vivo is regulated by Formin homology-2 domain containing 3 (FHOD3), which is activated by RhoA\/ROCK, establishing a novel mechanism through which the RCP\u2013\u03b15\u03b21 pathway reprograms the actin cytoskeleton to promote invasive migration and local invasion in vivo.<\/jats:p>","DOI":"10.1083\/jcb.201502040","type":"journal-article","created":{"date-parts":[[2015,9,14]],"date-time":"2015-09-14T09:34:06Z","timestamp":1442223246000},"page":"1013-1031","update-policy":"https:\/\/doi.org\/10.1083\/jcb.crossmarkpolicy","source":"Crossref","is-referenced-by-count":109,"title":["\u03b15\u03b21 integrin recycling promotes Arp2\/3-independent cancer cell invasion via the formin FHOD3"],"prefix":"10.1083","volume":"210","author":[{"given":"Nikki R.","family":"Paul","sequence":"first","affiliation":[{"name":"Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer L.","family":"Allen","sequence":"additional","affiliation":[{"name":"Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Chapman","sequence":"additional","affiliation":[{"name":"Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria","family":"Morlan-Mairal","sequence":"additional","affiliation":[{"name":"Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Egor","family":"Zindy","sequence":"additional","affiliation":[{"name":"Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guillaume","family":"Jacquemet","sequence":"additional","affiliation":[{"name":"Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura","family":"Fernandez del Ama","sequence":"additional","affiliation":[{"name":"Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nermina","family":"Ferizovic","sequence":"additional","affiliation":[{"name":"Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David M.","family":"Green","sequence":"additional","affiliation":[{"name":"Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonathan D.","family":"Howe","sequence":"additional","affiliation":[{"name":"Medical Research Council Laboratory of Molecular Biology, Cambridge CB2 0QH, England, UK 3"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elisabeth","family":"Ehler","sequence":"additional","affiliation":[{"name":"Randall Division of Cell and Molecular Biophysics, Cardiovascular Division, BHF Research Excellence Centre, King\u2019s College London, London SE1 1UL, England, UK 2"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adam","family":"Hurlstone","sequence":"additional","affiliation":[{"name":"Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrick T.","family":"Caswell","sequence":"additional","affiliation":[{"name":"Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, England, UK 1"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"291","published-online":{"date-parts":[[2015,9,14]]},"reference":[{"key":"2023072308190449700_bib1","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/j.cell.2009.01.039","article-title":"A Mutant-p53\/Smad complex opposes p63 to empower TGF\u03b2-induced metastasis","volume":"137","author":"Adorno","year":"2009","journal-title":"Cell."},{"key":"2023072308190449700_bib2","doi-asserted-by":"publisher","first-page":"5006","DOI":"10.1091\/mbc.E08-01-0034","article-title":"Retrograde flow and myosin II activity within the leading cell edge deliver F-actin to the lamella to seed the formation of graded polarity actomyosin II filament bundles in migrating fibroblasts","volume":"19","author":"Anderson","year":"2008","journal-title":"Mol. Biol. Cell."},{"key":"2023072308190449700_bib3","doi-asserted-by":"publisher","first-page":"1069","DOI":"10.1172\/JCI67280","article-title":"Mutant p53-associated myosin-X upregulation promotes breast cancer invasion and metastasis","volume":"124","author":"Arjonen","year":"2014","journal-title":"J. Clin. Invest."},{"key":"2023072308190449700_bib4","doi-asserted-by":"publisher","first-page":"1005","DOI":"10.1016\/j.cub.2012.03.064","article-title":"FMNL2 drives actin-based protrusion and migration downstream of Cdc42","volume":"22","author":"Block","year":"2012","journal-title":"Curr. Biol."},{"key":"2023072308190449700_bib5","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1016\/j.ceb.2011.12.004","article-title":"Directed cell invasion and migration during metastasis","volume":"24","author":"Bravo-Cordero","year":"2012","journal-title":"Curr. Opin. Cell Biol."},{"key":"2023072308190449700_bib6","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1242\/jcs.107250","article-title":"Formins at a glance","volume":"126","author":"Breitsprecher","year":"2013","journal-title":"J. Cell Sci."},{"key":"2023072308190449700_bib7","doi-asserted-by":"publisher","first-page":"3695","DOI":"10.1242\/jcs.095810","article-title":"Integrin trafficking at a glance","volume":"125","author":"Bridgewater","year":"2012","journal-title":"J. Cell Sci."},{"key":"2023072308190449700_bib8","doi-asserted-by":"publisher","first-page":"831","DOI":"10.1083\/jcb.201009119","article-title":"Actin polymerization driven by WASH causes V-ATPase retrieval and vesicle neutralization before exocytosis","volume":"193","author":"Carnell","year":"2011","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib9","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1111\/j.1600-0854.2005.00362.x","article-title":"Integrin trafficking and the control of cell migration","volume":"7","author":"Caswell","year":"2006","journal-title":"Traffic."},{"key":"2023072308190449700_bib10","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1016\/j.tcb.2008.03.004","article-title":"Endocytic transport of integrins during cell migration and invasion","volume":"18","author":"Caswell","year":"2008","journal-title":"Trends Cell Biol."},{"key":"2023072308190449700_bib11","doi-asserted-by":"publisher","first-page":"496","DOI":"10.1016\/j.devcel.2007.08.012","article-title":"Rab25 associates with \u03b15\u03b21 integrin to promote invasive migration in 3D microenvironments","volume":"13","author":"Caswell","year":"2007","journal-title":"Dev. Cell."},{"key":"2023072308190449700_bib12","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1083\/jcb.200804140","article-title":"Rab-coupling protein coordinates recycling of \u03b15\u03b21 integrin and EGFR1 to promote cell migration in 3D microenvironments","volume":"183","author":"Caswell","year":"2008","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib13","doi-asserted-by":"publisher","first-page":"843","DOI":"10.1038\/nrm2799","article-title":"Integrins: masters and slaves of endocytic transport","volume":"10","author":"Caswell","year":"2009","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023072308190449700_bib14","doi-asserted-by":"publisher","first-page":"1893","DOI":"10.1172\/JCI31721","article-title":"An inducible mouse model for skin cancer reveals distinct roles for gain- and loss-of-function p53 mutations","volume":"117","author":"Caulin","year":"2007","journal-title":"J. Clin. Invest."},{"key":"2023072308190449700_bib15","doi-asserted-by":"publisher","first-page":"688","DOI":"10.1016\/j.celrep.2014.06.045","article-title":"Heterogeneous tumor subpopulations cooperate to drive invasion","volume":"8","author":"Chapman","year":"2014","journal-title":"Cell Reports."},{"key":"2023072308190449700_bib16","doi-asserted-by":"publisher","first-page":"560","DOI":"10.1016\/j.devcel.2012.08.008","article-title":"PKD controls \u03b1v\u03b23 integrin recycling and tumor cell invasive migration through its substrate Rabaptin-5","volume":"23","author":"Christoforides","year":"2012","journal-title":"Dev. Cell."},{"key":"2023072308190449700_bib17","doi-asserted-by":"publisher","first-page":"1708","DOI":"10.1126\/science.1064829","article-title":"Taking cell-matrix adhesions to the third dimension","volume":"294","author":"Cukierman","year":"2001","journal-title":"Science."},{"key":"2023072308190449700_bib18","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1038\/nrc2748","article-title":"Integrins in cancer: biological implications and therapeutic opportunities","volume":"10","author":"Desgrosellier","year":"2010","journal-title":"Nat. Rev. Cancer."},{"key":"2023072308190449700_bib19","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1002\/path.2748","article-title":"p53 mutation and loss have different effects on tumourigenesis in a novel mouse model of pleomorphic rhabdomyosarcoma","volume":"222","author":"Doyle","year":"2010","journal-title":"J. Pathol."},{"key":"2023072308190449700_bib20","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1016\/j.devcel.2011.11.008","article-title":"Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes\/lysosomes and drive cancer progression","volume":"22","author":"Dozynkiewicz","year":"2012","journal-title":"Dev. Cell."},{"key":"2023072308190449700_bib21","first-page":"20","article-title":"Computer control of microscopes using \u00b5Manager","volume":"Chapter 14","author":"Edelstein","year":"2010","journal-title":"Curr. Protoc. Mol. Biol."},{"key":"2023072308190449700_bib22","doi-asserted-by":"publisher","first-page":"e10","DOI":"10.14440\/jbm.2014.36","article-title":"Advanced methods of microscope control using \u03bcManager software","volume":"1","author":"Edelstein","year":"2014","journal-title":"J Biol Methods."},{"key":"2023072308190449700_bib23","doi-asserted-by":"publisher","first-page":"992","DOI":"10.1016\/j.cell.2011.11.016","article-title":"Cancer invasion and the microenvironment: plasticity and reciprocity","volume":"147","author":"Friedl","year":"2011","journal-title":"Cell."},{"key":"2023072308190449700_bib24","doi-asserted-by":"publisher","first-page":"777","DOI":"10.1038\/ncb2548","article-title":"Classifying collective cancer cell invasion","volume":"14","author":"Friedl","year":"2012","journal-title":"Nat. Cell Biol."},{"key":"2023072308190449700_bib25","doi-asserted-by":"publisher","first-page":"999","DOI":"10.1083\/jcb.200810060","article-title":"Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed","volume":"183","author":"Gardel","year":"2008","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib26","doi-asserted-by":"publisher","first-page":"38902","DOI":"10.1074\/jbc.M306229200","article-title":"Activation of the Rac-binding partner FHOD1 induces actin stress fibers via a ROCK-dependent mechanism","volume":"278","author":"Gasteier","year":"2003","journal-title":"J. Biol. Chem."},{"key":"2023072308190449700_bib27","doi-asserted-by":"publisher","first-page":"4089","DOI":"10.1096\/fj.12-224352","article-title":"The Arp2\/3 complex mediates multigeneration dendritic protrusions for efficient 3-dimensional cancer cell migration","volume":"27","author":"Giri","year":"2013","journal-title":"FASEB J."},{"key":"2023072308190449700_bib28","doi-asserted-by":"publisher","first-page":"1931","DOI":"10.1038\/nprot.2014.131","article-title":"Quantitative and unbiased analysis of directional persistence in cell migration","volume":"9","author":"Gorelik","year":"2014","journal-title":"Nat. Protoc."},{"key":"2023072308190449700_bib29","doi-asserted-by":"publisher","first-page":"27891","DOI":"10.1074\/jbc.M801800200","article-title":"The Diaphanous-related Formin FHOD1 associates with ROCK1 and promotes Src-dependent plasma membrane blebbing","volume":"283","author":"Hannemann","year":"2008","journal-title":"J. Biol. Chem."},{"key":"2023072308190449700_bib30","first-page":"3591","article-title":"Fos-transformation activates genes associated with invasion","volume":"9","author":"Hennigan","year":"1994","journal-title":"Oncogene."},{"key":"2023072308190449700_bib31","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1016\/S0092-8674(02)00971-6","article-title":"Integrins: bidirectional, allosteric signaling machines","volume":"110","author":"Hynes","year":"2002","journal-title":"Cell."},{"key":"2023072308190449700_bib32","doi-asserted-by":"publisher","first-page":"1159","DOI":"10.1083\/jcb.201005060","article-title":"Formin follows function: a muscle-specific isoform of FHOD3 is regulated by CK2 phosphorylation and promotes myofibril maintenance","volume":"191","author":"Iskratsch","year":"2010","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib33","doi-asserted-by":"publisher","first-page":"893","DOI":"10.1007\/s00018-012-1154-7","article-title":"Two distinct phosphorylation events govern the function of muscle FHOD3","volume":"70","author":"Iskratsch","year":"2013","journal-title":"Cell. Mol. Life Sci."},{"key":"2023072308190449700_bib34","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1016\/j.devcel.2013.11.003","article-title":"FHOD1 is needed for directed forces and adhesion maturation during cell spreading and migration","volume":"27","author":"Iskratsch","year":"2013","journal-title":"Dev. Cell."},{"key":"2023072308190449700_bib35","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1146\/annurev-cellbio-092910-154017","article-title":"Cooperation between integrins and growth factor receptors in signaling and endocytosis","volume":"27","author":"Ivaska","year":"2011","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"2023072308190449700_bib36","doi-asserted-by":"publisher","first-page":"917","DOI":"10.1083\/jcb.201302041","article-title":"RCP-driven \u03b15\u03b21 recycling suppresses Rac and promotes RhoA activity via the RacGAP1-IQGAP1 complex","volume":"202","author":"Jacquemet","year":"2013","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib37","doi-asserted-by":"publisher","first-page":"627","DOI":"10.1016\/j.ceb.2013.05.008","article-title":"Role of adhesion receptor trafficking in 3D cell migration","volume":"25","author":"Jacquemet","year":"2013","journal-title":"Curr. Opin. Cell Biol."},{"key":"2023072308190449700_bib38","doi-asserted-by":"publisher","first-page":"665","DOI":"10.1111\/j.1365-2443.2005.00867.x","article-title":"Fhos2, a novel formin-related actin-organizing protein, probably associates with the nestin intermediate filament","volume":"10","author":"Kanaya","year":"2005","journal-title":"Genes Cells."},{"key":"2023072308190449700_bib39","first-page":"615","article-title":"Identification and characterization of human FHOD3 gene in silico","volume":"13","author":"Katoh","year":"2004","journal-title":"Int. J. Mol. Med."},{"key":"2023072308190449700_bib40","doi-asserted-by":"publisher","first-page":"2184","DOI":"10.2353\/ajpath.2009.090028","article-title":"beta3-integrin expression on tumor cells inhibits tumor progression, reduces metastasis, and is associated with a favorable prognosis in patients with ovarian cancer","volume":"175","author":"Kaur","year":"2009","journal-title":"Am. J. Pathol."},{"key":"2023072308190449700_bib41","doi-asserted-by":"publisher","first-page":"2441","DOI":"10.1038\/onc.2009.515","article-title":"Formin-like 2 drives amoeboid invasive cell motility downstream of RhoC","volume":"29","author":"Kitzing","year":"2010","journal-title":"Oncogene."},{"key":"2023072308190449700_bib42","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1038\/nrm3861","article-title":"Steering cell migration: lamellipodium dynamics and the regulation of directional persistence","volume":"15","author":"Krause","year":"2014","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023072308190449700_bib43","doi-asserted-by":"publisher","first-page":"982","DOI":"10.1038\/emboj.2008.34","article-title":"Arp2\/3 complex interactions and actin network turnover in lamellipodia","volume":"27","author":"Lai","year":"2008","journal-title":"EMBO J."},{"key":"2023072308190449700_bib44","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1083\/jcb.201304051","article-title":"Lamellipodin and the Scar\/WAVE complex cooperate to promote cell migration in vivo","volume":"203","author":"Law","year":"2013","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib45","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1101\/gad.1758709","article-title":"Genetic and cell biological analysis of integrin outside-in signaling","volume":"23","author":"Legate","year":"2009","journal-title":"Genes Dev."},{"key":"2023072308190449700_bib46","doi-asserted-by":"publisher","first-page":"769","DOI":"10.1016\/S0896-6273(00)80097-5","article-title":"Myosin drives retrograde F-actin flow in neuronal growth cones","volume":"16","author":"Lin","year":"1996","journal-title":"Neuron."},{"key":"2023072308190449700_bib47","doi-asserted-by":"publisher","first-page":"2849","DOI":"10.1242\/dev.035246","article-title":"Wash functions downstream of Rho and links linear and branched actin nucleation factors","volume":"136","author":"Liu","year":"2009","journal-title":"Development."},{"key":"2023072308190449700_bib48","doi-asserted-by":"publisher","first-page":"1097","DOI":"10.1083\/jcb.146.5.1097","article-title":"Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction","volume":"146","author":"Mallavarapu","year":"1999","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib49","doi-asserted-by":"publisher","first-page":"867","DOI":"10.1038\/nature00848","article-title":"Mice deficient in the Rac activator Tiam1 are resistant to Ras-induced skin tumours","volume":"417","author":"Malliri","year":"2002","journal-title":"Nature."},{"key":"2023072308190449700_bib50","doi-asserted-by":"publisher","first-page":"446","DOI":"10.1038\/nrm2406","article-title":"Filopodia: molecular architecture and cellular functions","volume":"9","author":"Mattila","year":"2008","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023072308190449700_bib51","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1007\/s10735-004-4273-0","article-title":"Expression of \u03b1 V-associated integrin \u03b2 subunits in epithelial ovarian cancer and its relation to prognosis in patients treated with platinum-based regimens","volume":"36","author":"Maubant","year":"2005","journal-title":"J. Mol. Histol."},{"key":"2023072308190449700_bib52","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1016\/B978-0-12-391857-4.00009-4","article-title":"Methods for cell and particle tracking","volume":"504","author":"Meijering","year":"2012","journal-title":"Methods Enzymol."},{"key":"2023072308190449700_bib53","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1016\/j.bbamcr.2008.12.018","article-title":"The role of formins in filopodia formation","volume":"1803","author":"Mellor","year":"2010","journal-title":"Biochim. Biophys. Acta."},{"key":"2023072308190449700_bib54","doi-asserted-by":"publisher","first-page":"1327","DOI":"10.1016\/j.cell.2009.11.026","article-title":"Mutant p53 drives invasion by promoting integrin recycling","volume":"139","author":"Muller","year":"2009","journal-title":"Cell."},{"key":"2023072308190449700_bib55","doi-asserted-by":"publisher","first-page":"1252","DOI":"10.1038\/onc.2012.148","article-title":"Mutant p53 enhances MET trafficking and signalling to drive cell scattering and invasion","volume":"32","author":"Muller","year":"2013","journal-title":"Oncogene."},{"key":"2023072308190449700_bib56","doi-asserted-by":"publisher","first-page":"1031","DOI":"10.1038\/nature08231","article-title":"Characterization of two classes of small molecule inhibitors of Arp2\/3 complex","volume":"460","author":"Nolen","year":"2009","journal-title":"Nature."},{"key":"2023072308190449700_bib57","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1038\/nrc3003","article-title":"Nucleating actin for invasion","volume":"11","author":"N\u00fcrnberg","year":"2011","journal-title":"Nat. Rev. Cancer."},{"key":"2023072308190449700_bib58","doi-asserted-by":"publisher","first-page":"803","DOI":"10.1038\/ncb1437","article-title":"FilGAP, a Rho- and ROCK-regulated GAP for Rac binds filamin A to control actin remodelling","volume":"8","author":"Ohta","year":"2006","journal-title":"Nat. Cell Biol."},{"key":"2023072308190449700_bib59","doi-asserted-by":"crossref","first-page":"1918","DOI":"10.1523\/JNEUROSCI.11-07-01918.1991","article-title":"Actin dynamics in growth cones","volume":"11","author":"Okabe","year":"1991","journal-title":"J. Neurosci."},{"key":"2023072308190449700_bib60","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1016\/j.cub.2005.01.011","article-title":"The Rho family GTPase Rif induces filopodia through mDia2","volume":"15","author":"Pellegrin","year":"2005","journal-title":"Curr. Biol."},{"key":"2023072308190449700_bib61","doi-asserted-by":"publisher","first-page":"3723","DOI":"10.1242\/jcs.03216","article-title":"Integrin traffic","volume":"119","author":"Pellinen","year":"2006","journal-title":"J. Cell Sci."},{"key":"2023072308190449700_bib62","doi-asserted-by":"publisher","first-page":"534","DOI":"10.1016\/S0960-9822(03)00170-2","article-title":"Disruption of the Diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 as an effector for Cdc42","volume":"13","author":"Peng","year":"2003","journal-title":"Curr. Biol."},{"key":"2023072308190449700_bib63","doi-asserted-by":"publisher","first-page":"439","DOI":"10.1083\/jcb.201201124","article-title":"Nonpolarized signaling reveals two distinct modes of 3D cell migration","volume":"197","author":"Petrie","year":"2012","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib64","doi-asserted-by":"publisher","first-page":"1062","DOI":"10.1126\/science.1256965","article-title":"Generation of compartmentalized pressure by a nuclear piston governs cell motility in a 3D matrix","volume":"345","author":"Petrie","year":"2014","journal-title":"Science."},{"key":"2023072308190449700_bib65","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1083\/jcb.201109112","article-title":"Diacylglycerol kinase \u03b1 controls RCP-dependent integrin trafficking to promote invasive migration","volume":"196","author":"Rainero","year":"2012","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib66","doi-asserted-by":"publisher","first-page":"605","DOI":"10.1038\/nmeth.1220","article-title":"Lifeact: a versatile marker to visualize F-actin","volume":"5","author":"Riedl","year":"2008","journal-title":"Nat. Methods."},{"key":"2023072308190449700_bib67","doi-asserted-by":"publisher","first-page":"1158","DOI":"10.1016\/j.chembiol.2009.10.006","article-title":"Identification and characterization of a small molecule inhibitor of formin-mediated actin assembly","volume":"16","author":"Rizvi","year":"2009","journal-title":"Chem. Biol."},{"key":"2023072308190449700_bib68","doi-asserted-by":"publisher","first-page":"510","DOI":"10.1016\/j.cell.2008.09.043","article-title":"Rac activation and inactivation control plasticity of tumor cell movement","volume":"135","author":"Sanz-Moreno","year":"2008","journal-title":"Cell."},{"key":"2023072308190449700_bib69","doi-asserted-by":"publisher","first-page":"2329","DOI":"10.1158\/0008-5472.CAN-07-5167","article-title":"Loss of E-cadherin promotes ovarian cancer metastasis via \u03b15-integrin, which is a therapeutic target","volume":"68","author":"Sawada","year":"2008","journal-title":"Cancer Res."},{"key":"2023072308190449700_bib70","doi-asserted-by":"publisher","first-page":"1101","DOI":"10.1038\/nprot.2008.73","article-title":"Analyzing real-time PCR data by the comparative C(T) method","volume":"3","author":"Schmittgen","year":"2008","journal-title":"Nat. Protoc."},{"key":"2023072308190449700_bib71","doi-asserted-by":"publisher","first-page":"706","DOI":"10.1158\/2159-8290.CD-11-0239","article-title":"The outgrowth of micrometastases is enabled by the formation of filopodium-like protrusions","volume":"2","author":"Shibue","year":"2012","journal-title":"Cancer Discov."},{"key":"2023072308190449700_bib72","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1016\/j.ccr.2013.08.012","article-title":"An integrin-linked machinery of cytoskeletal regulation that enables experimental tumor initiation and metastatic colonization","volume":"24","author":"Shibue","year":"2013","journal-title":"Cancer Cell."},{"key":"2023072308190449700_bib73","doi-asserted-by":"publisher","first-page":"1047","DOI":"10.1016\/j.cell.2009.04.013","article-title":"Cyfip1 is a putative invasion suppressor in epithelial cancers","volume":"137","author":"Silva","year":"2009","journal-title":"Cell."},{"key":"2023072308190449700_bib74","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1083\/jcb.201112113","article-title":"The Arp2\/3 complex is required for lamellipodia extension and directional fibroblast cell migration","volume":"197","author":"Suraneni","year":"2012","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib75","doi-asserted-by":"publisher","first-page":"901","DOI":"10.1091\/mbc.E14-07-1250","article-title":"A mechanism of leading-edge protrusion in the absence of Arp2\/3 complex","volume":"26","author":"Suraneni","year":"2015","journal-title":"Mol. Biol. Cell."},{"key":"2023072308190449700_bib76","doi-asserted-by":"publisher","first-page":"618","DOI":"10.1038\/emboj.2008.7","article-title":"The mammalian formin FHOD1 is activated through phosphorylation by ROCK and mediates thrombin-induced stress fibre formation in endothelial cells","volume":"27","author":"Takeya","year":"2008","journal-title":"EMBO J."},{"key":"2023072308190449700_bib77","doi-asserted-by":"publisher","first-page":"29873","DOI":"10.1074\/jbc.M109.059303","article-title":"Mammalian formin fhod3 regulates actin assembly and sarcomere organization in striated muscles","volume":"284","author":"Taniguchi","year":"2009","journal-title":"J. Biol. Chem."},{"key":"2023072308190449700_bib78","doi-asserted-by":"publisher","first-page":"3481","DOI":"10.1007\/s00018-012-1251-7","article-title":"Collective cell migration of epithelial and mesenchymal cells","volume":"70","author":"Theveneau","year":"2013","journal-title":"Cell. Mol. Life Sci."},{"key":"2023072308190449700_bib79","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1083\/jcb.201303129","article-title":"Vinculin-actin interaction couples actin retrograde flow to focal adhesions, but is dispensable for focal adhesion growth","volume":"202","author":"Thievessen","year":"2013","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib80","doi-asserted-by":"publisher","first-page":"751","DOI":"10.1038\/ncb2775","article-title":"Matrix geometry determines optimal cancer cell migration strategy and modulates response to interventions","volume":"15","author":"Tozluo\u011flu","year":"2013","journal-title":"Nat. Cell Biol."},{"key":"2023072308190449700_bib81","doi-asserted-by":"publisher","first-page":"443","DOI":"10.1083\/jcb.201306067","article-title":"CellGeo: a computational platform for the analysis of shape changes in cells with complex geometries","volume":"204","author":"Tsygankov","year":"2014","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib82","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1016\/j.celrep.2014.12.012","article-title":"HUWE1 ubiquitylates and degrades the RAC activator TIAM1 promoting cell-cell adhesion disassembly, migration, and invasion","volume":"10","author":"Vaughan","year":"2015","journal-title":"Cell Reports."},{"key":"2023072308190449700_bib83","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1083\/jcb.201011038","article-title":"RhoA and RhoC have distinct roles in migration and invasion by acting through different targets","volume":"193","author":"Vega","year":"2011","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib84","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1083\/jcb.200609004","article-title":"\u03b1v\u03b23 and \u03b15\u03b21 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration","volume":"177","author":"White","year":"2007","journal-title":"J. Cell Biol."},{"key":"2023072308190449700_bib85","doi-asserted-by":"publisher","first-page":"973","DOI":"10.1016\/j.cell.2011.12.034","article-title":"Arp2\/3 is critical for lamellipodia and response to extracellular matrix cues but is dispensable for chemotaxis","volume":"148","author":"Wu","year":"2012","journal-title":"Cell."},{"key":"2023072308190449700_bib86","doi-asserted-by":"publisher","first-page":"3753","DOI":"10.1242\/jcs.080986","article-title":"The Arp2\/3 activator WASH regulates \u03b15\u03b21-integrin-mediated invasive migration","volume":"124","author":"Zech","year":"2011","journal-title":"J. Cell Sci."}],"container-title":["Journal of Cell Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/rupress.org\/jcb\/article-pdf\/210\/6\/1013\/1593323\/jcb_201502040.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/rupress.org\/jcb\/article-pdf\/210\/6\/1013\/1593323\/jcb_201502040.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,23]],"date-time":"2023-07-23T04:21:08Z","timestamp":1690086068000},"score":1,"resource":{"primary":{"URL":"https:\/\/rupress.org\/jcb\/article\/210\/6\/1013\/38233\/5-1-integrin-recycling-promotes-Arp2-3-independent"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,9,14]]},"references-count":86,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2015,9,14]]}},"URL":"https:\/\/doi.org\/10.1083\/jcb.201502040","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.725788040.793510040","asserted-by":"object"}]},"ISSN":["0021-9525","1540-8140"],"issn-type":[{"value":"0021-9525","type":"print"},{"value":"1540-8140","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,9,14]]}}}