{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T01:18:37Z","timestamp":1788311917788,"version":"build-2803163510"},"reference-count":105,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2024,9,30]],"date-time":"2024-09-30T00:00:00Z","timestamp":1727654400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100009845","name":"Ovarian Cancer Research Foundation","doi-asserted-by":"publisher","award":["GA-2019-20"],"award-info":[{"award-number":["GA-2019-20"]}],"id":[{"id":"10.13039\/100009845","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Victorian Government\u2019s Operational Infrastructure Support Program","award":["GA-2019-20"],"award-info":[{"award-number":["GA-2019-20"]}]},{"name":"Australian Government Research Training Program (RTP) Scholarship","award":["GA-2019-20"],"award-info":[{"award-number":["GA-2019-20"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Metastasis is the leading cause of cancer-related mortality; however, a complete understanding of the molecular programs driving the metastatic cascade is lacking. Metastasis is dependent on collective invasion\u2014a developmental process exploited by many epithelial cancers to establish secondary tumours and promote widespread disease. The key drivers of collective invasion are \u201cLeader Cells\u201d, a functionally distinct subpopulation of cells that direct migration, cellular contractility, and lead trailing or follower cells. While a significant body of research has focused on leader cell biology in the traditional context of collective invasion, the influence of metastasis-promoting leader cells is an emerging area of study. This review provides insights into the expanded role of leader cells, detailing emerging evidence on the hybrid epithelial\u2013mesenchymal transition (EMT) state and the phenotypical plasticity exhibited by leader cells. Additionally, we explore the role of leader cells in chemotherapeutic resistance and immune evasion, highlighting their potential as effective and diverse targets for novel cancer therapies.<\/jats:p>","DOI":"10.3390\/ijms251910554","type":"journal-article","created":{"date-parts":[[2024,9,30]],"date-time":"2024-09-30T10:00:47Z","timestamp":1727690447000},"page":"10554","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Leader Cells: Invade and Evade\u2014The Frontline of Cancer Progression"],"prefix":"10.3390","volume":"25","author":[{"given":"Brittany R.","family":"Doran","sequence":"first","affiliation":[{"name":"Hudson Institute of Medical Research, Clayton 3168, Australia"},{"name":"Department of Molecular and Translational Sciences, Monash University, Clayton 3168, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura R.","family":"Moffitt","sequence":"additional","affiliation":[{"name":"Hudson Institute of Medical Research, Clayton 3168, Australia"},{"name":"Department of Molecular and Translational Sciences, Monash University, Clayton 3168, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amy L.","family":"Wilson","sequence":"additional","affiliation":[{"name":"Hudson Institute of Medical Research, Clayton 3168, Australia"},{"name":"Department of Molecular and Translational Sciences, Monash University, Clayton 3168, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew N.","family":"Stephens","sequence":"additional","affiliation":[{"name":"Hudson Institute of Medical Research, Clayton 3168, Australia"},{"name":"Department of Molecular and Translational Sciences, Monash University, Clayton 3168, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6319-1153","authenticated-orcid":false,"given":"Maree","family":"Bilandzic","sequence":"additional","affiliation":[{"name":"Hudson Institute of Medical Research, Clayton 3168, Australia"},{"name":"Department of Molecular and Translational Sciences, Monash University, Clayton 3168, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,9,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"578","DOI":"10.1038\/s41568-024-00708-4","article-title":"Why do patients with cancer die?","volume":"24","author":"Boire","year":"2024","journal-title":"Nat. Rev. Cancer"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"100773","DOI":"10.1016\/j.tranon.2020.100773","article-title":"Epithelial-Mesenchymal Transition in Cancer: A Historical Overview","volume":"13","author":"Ribatti","year":"2020","journal-title":"Transl. Oncol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1038\/nrc.2017.118","article-title":"EMT in cancer","volume":"18","author":"Brabletz","year":"2018","journal-title":"Nat. Rev. Cancer"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1038\/nrm.2015.14","article-title":"The front and rear of collective cell migration","volume":"17","author":"Mayor","year":"2016","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Lu, P., and Lu, Y. (2021). Born to Run? Diverse Modes of Epithelial Migration. Front. Cell Dev. Biol., 9.","DOI":"10.3389\/fcell.2021.704939"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3535","DOI":"10.1007\/s00018-016-2260-8","article-title":"Adherens Junction and E-Cadherin complex regulation by epithelial polarity","volume":"73","author":"Coopman","year":"2016","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1038\/s41580-018-0080-4","article-title":"New insights into the mechanisms of epithelial-mesenchymal transition and implications for cancer","volume":"20","author":"Dongre","year":"2018","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1126\/science.aaf6546","article-title":"A collective route to metastasis: Seeding by tumor cell clusters","volume":"352","author":"Cheung","year":"2016","journal-title":"Science"},{"key":"ref_9","doi-asserted-by":"crossref","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":"ref_10","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1091\/mbc.E20-10-0681","article-title":"Roles of leader and follower cells in collective cell migration","volume":"32","author":"Qin","year":"2021","journal-title":"Mol. Biol. Cell"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"100845","DOI":"10.1016\/j.tranon.2020.100845","article-title":"Hypoxia, partial EMT and collective migration: Emerging culprits in metastasis","volume":"13","author":"Saxena","year":"2020","journal-title":"Transl. Oncol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1899","DOI":"10.12688\/f1000research.11889.1","article-title":"Leaders in collective migration: Are front cells really endowed with a particular set of skills?","volume":"6","author":"Theveneau","year":"2017","journal-title":"F1000Research"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"115","DOI":"10.3892\/ijo.2023.5563","article-title":"Tumour follower cells: A novel driver of leader cells in collective invasion (Review)","volume":"63","author":"Wang","year":"2023","journal-title":"Int. J. Oncol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Moffitt, L., Karimnia, N., Stephens, A., and Bilandzic, M. (2019). Therapeutic Targeting of Collective Invasion in Ovarian Cancer. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20061466"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1639","DOI":"10.1016\/j.cell.2013.11.029","article-title":"Collective Invasion in Breast Cancer Requires a Conserved Basal Epithelial Program","volume":"155","author":"Cheung","year":"2013","journal-title":"Cell"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1038\/s41568-021-00376-8","article-title":"Decoding leader cells in collective cancer invasion","volume":"21","author":"Bocci","year":"2021","journal-title":"Nat. Rev. Cancer"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Bilandzic, M., Rainczuk, A., Green, E., Fairweather, N., Jobling, T.W., Plebanski, M., and Stephens, A.N. (2019). Keratin-14 (KRT14) Positive Leader Cells Mediate Mesothelial Clearance and Invasion by Ovarian Cancer Cells. Cancers, 11.","DOI":"10.3390\/cancers11091228"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"103917","DOI":"10.1016\/j.isci.2022.103917","article-title":"Single cell analysis of mechanical properties and EMT-related gene expression profiles in cancer fingers","volume":"25","author":"Zou","year":"2022","journal-title":"iScience"},{"key":"ref_19","first-page":"1233","article-title":"Cathepsin B defines leader cells during the collective invasion of salivary adenoid cystic carcinoma","volume":"54","author":"Wu","year":"2019","journal-title":"Int. J. Oncol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Gao, X.-L., Wu, J.-S., Cao, M.-X., Gao, S.-Y., Cen, X., Jiang, Y.-P., Wang, S.-S., Tang, Y.-J., Chen, Q.-M., and Liang, X.-H. (2017). Cytokeratin-14 contributes to collective invasion of salivary adenoid cystic carcinoma. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0171341"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3140","DOI":"10.1002\/cncr.32903","article-title":"Prognostic significance of an invasive leader cell\u2013derived mutation cluster on chromosome 16q","volume":"126","author":"Pedro","year":"2020","journal-title":"Cancer"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"10788","DOI":"10.1073\/pnas.1834401100","article-title":"Rho-dependent formation of epithelial \u201cleader\u201d cells during wound healing","volume":"100","author":"Omelchenko","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"15988","DOI":"10.1073\/pnas.0705062104","article-title":"Collective migration of an epithelial monolayer in response to a model wound","volume":"104","author":"Poujade","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1111\/cas.14285","article-title":"Cancer stem-like cells with hybrid epithelial\/mesenchymal phenotype leading the collective invasion","volume":"111","author":"Quan","year":"2020","journal-title":"Cancer Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1016\/j.ceb.2019.10.001","article-title":"Multicellular scale front-to-rear polarity in collective migration","volume":"62","author":"Capuana","year":"2020","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/j.yexcr.2019.01.006","article-title":"Cadherin mechanotransduction in leader-follower cell specification during collective migration","volume":"376","author":"Khalil","year":"2019","journal-title":"Exp. Cell Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1038\/ncb2917","article-title":"Interplay of RhoA and mechanical forces in collective cell migration driven by leader cells","volume":"16","author":"Reffay","year":"2014","journal-title":"Nat. Cell Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1146","DOI":"10.1016\/j.cell.2014.03.045","article-title":"Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration","volume":"157","author":"Cai","year":"2014","journal-title":"Cell"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.ceb.2017.06.006","article-title":"Actomyosin contractility and collective migration: May the force be with you","volume":"48","author":"Pandya","year":"2017","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e983869","DOI":"10.4161\/sgtp.28997","article-title":"Rho GTPases in collective cell migration","volume":"5","author":"Zegers","year":"2014","journal-title":"Small GTPases"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Yamaguchi, N., Mizutani, T., Kawabata, K., and Haga, H. (2015). Leader cells regulate collective cell migration via Rac activation in the downstream signaling of integrin \u03b21 and PI3K. Sci. Rep., 5.","DOI":"10.1038\/srep07656"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"568","DOI":"10.1039\/c0ib00052c","article-title":"Determinants of leader cells in collective cell migration","volume":"2","author":"Khalil","year":"2010","journal-title":"Integr. Biol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1899","DOI":"10.1158\/0008-5472.CAN-18-2828","article-title":"Randomly Distributed K14+ Breast Tumor Cells Polarize to the Leading Edge and Guide Collective Migration in Response to Chemical and Mechanical Environmental Cues","volume":"79","author":"Hwang","year":"2019","journal-title":"Cancer Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2570","DOI":"10.1016\/j.cub.2019.06.061","article-title":"Cadherin-Mediated Cell Coupling Coordinates Chemokine Sensing across Collectively Migrating Cells","volume":"29","author":"Lan","year":"2019","journal-title":"Curr. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"15078","DOI":"10.1038\/ncomms15078","article-title":"Image-guided genomics of phenotypically heterogeneous populations reveals vascular signalling during sym-biotic collective cancer invasion","volume":"8","author":"Konen","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3469","DOI":"10.1038\/s41467-018-05927-6","article-title":"Mechanical interactions among followers determine the emergence of leaders in migrating epithelial cell collectives","volume":"9","author":"Vishwakarma","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1242\/jcs.01577","article-title":"Multiple rows of cells behind an epithelial wound edge extend cryptic lamellipodia to collectively drive cell-sheet movement","volume":"118","author":"Farooqui","year":"2005","journal-title":"J. Cell Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"943","DOI":"10.1038\/ncb2103","article-title":"Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting","volume":"12","author":"Jakobsson","year":"2010","journal-title":"Nat. Cell Biol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Poltavets, V., Kochetkova, M., Pitson, S.M., and Samuel, M.S. (2018). The Role of the Extracellular Matrix and Its Molecular and Cellular Regulators in Cancer Cell Plasticity. Front. Oncol., 8.","DOI":"10.3389\/fonc.2018.00431"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"S20","DOI":"10.1097\/IJG.0000000000000108","article-title":"Biology of the extracellular matrix: An overview","volume":"23","author":"Yue","year":"2014","journal-title":"J. Glaucoma"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"5120","DOI":"10.1038\/s41467-020-18794-x","article-title":"Concepts of extracellular matrix remodelling in tumour progression and metastasis","volume":"11","author":"Winkler","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1016\/j.devcel.2019.03.026","article-title":"The Extracellular Matrix Modulates the Metastatic Journey","volume":"49","author":"Kai","year":"2019","journal-title":"Dev. Cell"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1007\/s10585-013-9565-x","article-title":"Leading malignant cells initiate collective epithelial cell invasion in a three-dimensional heterotypic tumor spheroid model","volume":"30","author":"Carey","year":"2013","journal-title":"Clin. Exp. Metastasis"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1615","DOI":"10.1158\/1541-7786.MCR-20-0334","article-title":"Tumor-Resident Stromal Cells Promote Breast Cancer Invasion through Regulation of the Basal Phenotype","volume":"18","author":"Hanley","year":"2020","journal-title":"Mol. Cancer Res."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Ansardamavandi, A., and Tafazzoli-Shadpour, M. (2021). The functional cross talk between cancer cells and cancer associated fibroblasts from a cancer mechanics perspective. Biochim. Biophys. Acta (BBA) Mol. Cell Res., 1868.","DOI":"10.1016\/j.bbamcr.2021.119103"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"2871","DOI":"10.1007\/s13277-013-1511-7","article-title":"Collagen as a double-edged sword in tumor progression","volume":"35","author":"Fang","year":"2013","journal-title":"Tumor Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1073\/pnas.1118910109","article-title":"Mechanical compression drives cancer cells toward invasive phenotype","volume":"109","author":"Tse","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2458","DOI":"10.1038\/s41388-022-02258-1","article-title":"Spatial collagen stiffening promotes collective breast cancer cell invasion by reinforcing extracellular matrix alignment","volume":"41","author":"Koorman","year":"2022","journal-title":"Oncogene"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"4597","DOI":"10.1158\/0008-5472.CAN-13-3698","article-title":"Force engages vinculin and promotes tumor progression by enhancing PI3K activation of phosphati-dylinositol (3,4,5)-triphosphate","volume":"74","author":"Rubashkin","year":"2014","journal-title":"Cancer Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1016\/j.cell.2009.10.027","article-title":"Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling","volume":"139","author":"Levental","year":"2009","journal-title":"Cell"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.jons.2017.06.002","article-title":"Biology of glucose metabolization in cancer cells","volume":"3","author":"Fadaka","year":"2017","journal-title":"J. Oncol. Sci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/j.tcb.2021.01.006","article-title":"Fueling Cell Invasion through Extracellular Matrix","volume":"31","author":"Garde","year":"2021","journal-title":"Trends Cell Biol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1533","DOI":"10.1038\/s41467-020-15219-7","article-title":"Subpopulation targeting of pyruvate dehydrogenase and GLUT1 decouples metabolic heterogeneity during collective cancer cell invasion","volume":"11","author":"Commander","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1038\/s41556-020-0477-0","article-title":"Transcriptional diversity and bioenergetic shift in human breast cancer metastasis revealed by single-cell RNA sequencing","volume":"22","author":"Davis","year":"2020","journal-title":"Nat. Cell Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1091\/mbc.E17-01-0041","article-title":"Regulation of ATP utilization during metastatic cell migration by collagen architecture","volume":"29","author":"Zanotelli","year":"2018","journal-title":"Mol. Biol. Cell"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"7867","DOI":"10.1073\/pnas.1809964116","article-title":"Energetic regulation of coordinated leader\u2013follower dynamics during collective invasion of breast cancer cells","volume":"116","author":"Zhang","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"jcs227116","DOI":"10.1242\/jcs.227116","article-title":"Invadopodia-mediated ECM degradation is enhanced in the G1 phase of the cell cycle","volume":"132","author":"Bayarmagnai","year":"2019","journal-title":"J. Cell Sci."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"992","DOI":"10.1038\/ncb3039","article-title":"PGC-1\u03b1 mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to pro-mote metastasis","volume":"16","author":"LeBleu","year":"2014","journal-title":"Nat. Cell Biol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"24980","DOI":"10.18632\/oncotarget.25166","article-title":"Biological and metabolic effects of IACS-010759, an OxPhos inhibitor, on chronic lymphocytic leukemia cells","volume":"9","author":"Vangapandu","year":"2018","journal-title":"Oncotarget"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"2662","DOI":"10.1091\/mbc.e16-05-0286","article-title":"AMPK activity regulates trafficking of mitochondria to the leading edge during cell migration and matrix invasion","volume":"27","author":"Cunniff","year":"2016","journal-title":"Mol. Biol. Cell"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"ra80","DOI":"10.1126\/scisignal.aab1624","article-title":"Survivin promotes oxidative phosphorylation, subcellular mitochondrial repositioning, and tumor cell invasion","volume":"8","author":"Rivadeneira","year":"2015","journal-title":"Sci. Signal."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"2159","DOI":"10.1091\/mbc.e16-10-0741","article-title":"Miro1-mediated mitochondrial positioning shapes intracellular energy gradients required for cell migration","volume":"28","author":"Schuler","year":"2017","journal-title":"Mol. Biol. Cell"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"8638","DOI":"10.1073\/pnas.1500722112","article-title":"PI3K therapy reprograms mitochondrial trafficking to fuel tumor cell invasion","volume":"112","author":"Caino","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"4814","DOI":"10.1038\/onc.2012.494","article-title":"Mitochondrial dynamics regulates migration and invasion of breast cancer cells","volume":"32","author":"Zhao","year":"2013","journal-title":"Oncogene"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"E854","DOI":"10.1073\/pnas.1508541113","article-title":"Polyclonal breast cancer metastases arise from collective dissemination of keratin 14-expressing tumor cell clusters","volume":"113","author":"Cheung","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1186\/s13046-021-02086-3","article-title":"Chemoresistance is mediated by ovarian cancer leader cells in vitro","volume":"40","author":"Karimnia","year":"2021","journal-title":"J. Exp. Clin. Cancer Res."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1038\/nature14034","article-title":"Blocking PGE2-induced tumour repopulation abrogates bladder cancer chemoresistance","volume":"517","author":"Kurtova","year":"2015","journal-title":"Nature"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"6354","DOI":"10.1038\/s41388-019-0889-0","article-title":"Keratin 14-high subpopulation mediates lung cancer metastasis potentially through Gkn1 upregulation","volume":"38","author":"Yao","year":"2019","journal-title":"Oncogene"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"4068","DOI":"10.1091\/mbc.e10-08-0703","article-title":"Novel function of keratins 5 and 14 in proliferation and differentiation of stratified epithelial cells","volume":"22","author":"Alam","year":"2011","journal-title":"Mol. Biol. Cell"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Jung, M., Jang, I., Kim, K., and Moon, K.C. (2020). CK14 Expression Identifies a Basal\/Squamous-Like Type of Papillary Non-Muscle-Invasive Upper Tract Urothelial Carcinoma. Front. Oncol., 10.","DOI":"10.3389\/fonc.2020.00623"},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Sonzogni, O., Haynes, J., Seifried, L.A., Kamel, Y.M., Huang, K., BeGora, M.D., Yeung, F.A., Robert-Tissot, C., Heng, Y.J., and Yuan, X. (2018). Reporters to mark and eliminate basal or luminal epithelial cells in culture and in vivo. PLoS Biol., 16.","DOI":"10.1371\/journal.pbio.2004049"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"4866","DOI":"10.1038\/s41467-024-49230-z","article-title":"A YAP-centered mechanotransduction loop drives collective breast cancer cell invasion","volume":"15","author":"Khalil","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Infante, E., and Etienne-Manneville, S. (2022). Intermediate filaments: Integration of cell mechanical properties during migration. Front. Cell Dev. Biol., 10.","DOI":"10.3389\/fcell.2022.951816"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1796","DOI":"10.12688\/f1000research.15967.1","article-title":"Vimentin on the move: New developments in cell migration","volume":"7","author":"Battaglia","year":"2018","journal-title":"F1000Research"},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Parvanian, S., Coelho-Rato, L.S., Patteson, A.E., and Eriksson, J.E. (2023). Vimentin takes a hike\u2014Emerging roles of extracellular vimentin in cancer and wound healing. Curr. Opin. Cell Biol., 85.","DOI":"10.1016\/j.ceb.2023.102246"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1016\/j.semcancer.2021.12.006","article-title":"Vimentin and cytokeratin: Good alone, bad together","volume":"86","author":"Kuburich","year":"2022","journal-title":"Semin. Cancer Biol."},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Ostrowska-Podhorodecka, Z., Ding, I., Norouzi, M., and McCulloch, C.A. (2022). Impact of Vimentin on Regulation of Cell Signaling and Matrix Remodeling. Front. Cell Dev. Biol., 10.","DOI":"10.3389\/fcell.2022.869069"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"3031","DOI":"10.1083\/jcb.201801162","article-title":"Intermediate filaments control collective migration by restricting traction forces and sustaining cell-cell contacts","volume":"217","author":"Seetharaman","year":"2018","journal-title":"J. Cell Biol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1274","DOI":"10.1091\/mbc.e10-08-0699","article-title":"Vimentin organization modulates the formation of lamellipodia","volume":"22","author":"Helfand","year":"2011","journal-title":"Mol. Biol. Cell"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"15966","DOI":"10.18632\/oncotarget.3862","article-title":"Vimentin contributes to epithelial-mesenchymal transition cancer cell mechanics by mediating cytoskeletal organization and focal adhesion maturation","volume":"6","author":"Liu","year":"2015","journal-title":"Oncotarget"},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Dmello, C., Sawant, S., Alam, H., Gangadaran, P., Mogre, S., Tiwari, R., D\u2019souza, Z., Narkar, M., Thorat, R., and Patil, K. (2017). Vimentin regulates differentiation switch via modulation of keratin 14 levels and their expression together correlates with poor prognosis in oral cancer patients. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0172559"},{"key":"ref_82","doi-asserted-by":"crossref","unstructured":"Velez-delValle, C., Marsch-Moreno, M., Castro-Mu\u00f1ozledo, F., Galv\u00e1n-Mendoza, I.J., and Kuri-Harcuch, W. (2016). Epithelial cell migration requires the interaction between the vimentin and keratin intermediate filaments. Sci. Rep., 6.","DOI":"10.1038\/srep24389"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"2148","DOI":"10.1242\/jcs.080127","article-title":"Keratin 8 phosphorylation regulates keratin reorganization and migration of epithelial tumor cells","volume":"125","author":"Busch","year":"2012","journal-title":"J. Cell Sci."},{"key":"ref_84","first-page":"2161","article-title":"Nestin regulates prostate cancer cell invasion by influencing the localisation and functions of FAK and integrins","volume":"127","author":"Hyder","year":"2014","journal-title":"J. Cell Sci."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"1698","DOI":"10.1091\/mbc.e09-05-0373","article-title":"Keratin 8\/18 modulation of protein kinase C-mediated integrin-dependent adhesion and migration of liver epithelial cells","volume":"21","author":"Bordeleau","year":"2010","journal-title":"Mol. Biol. Cell"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"2096","DOI":"10.1242\/jcs.073585","article-title":"Loss of keratins 8 and 18 leads to alterations in \u03b16\u03b24-integrin-mediated signalling and decreased neoplastic progression in an oral-tumour-derived cell line","volume":"124","author":"Alam","year":"2011","journal-title":"J. Cell Sci."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"jcs243956","DOI":"10.1242\/jcs.243956","article-title":"Disease-associated keratin mutations reduce traction forces and compromise adhesion and collective migration","volume":"133","author":"Fujiwara","year":"2020","journal-title":"J. Cell Sci."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"7113","DOI":"10.1038\/s41388-019-0899-y","article-title":"Inducible formation of leader cells driven by CD44 switching gives rise to collective invasion and metastases in luminal breast carcinomas","volume":"38","author":"Yang","year":"2019","journal-title":"Oncogene"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"28592","DOI":"10.18632\/oncotarget.8696","article-title":"\u0394Np63\u03b1 induces the expression of FAT2 and Slug to promote tumor invasion","volume":"7","author":"Dang","year":"2016","journal-title":"Oncotarget"},{"key":"ref_90","doi-asserted-by":"crossref","unstructured":"Latifi, A., Luwor, R.B., Bilandzic, M., Nazaretian, S., Stenvers, K., Pyman, J., Zhu, H., Thompson, E.W., Quinn, M.A., and Findlay, J.K. (2012). Isolation and Characterization of Tumor Cells from the Ascites of Ovarian Cancer Patients: Molecular Phenotype of Chemoresistant Ovarian Tumors. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0046858"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"12819","DOI":"10.1038\/ncomms12819","article-title":"Metastatic progression is associated with dynamic changes in the local microenvironment","volume":"7","author":"Aiello","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1016\/j.tcb.2018.12.001","article-title":"EMT Transition States during Tumor Progression and Metastasis","volume":"29","author":"Pastushenko","year":"2019","journal-title":"Trends Cell Biol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1016\/j.stemcr.2017.07.004","article-title":"SOX2 Is a Marker for Stem-like Tumor Cells in Bladder Cancer","volume":"9","author":"Zhu","year":"2017","journal-title":"Stem Cell Rep."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1158\/1535-7163.MCT-18-0584","article-title":"Circulating Tumor Cells with Stemness and Epithelial-to-Mesenchymal Transition Features Are Chemoresistant and Predictive of Poor Outcome in Metastatic Breast Cancer","volume":"18","author":"Papadaki","year":"2019","journal-title":"Mol. Cancer Ther."},{"key":"ref_95","doi-asserted-by":"crossref","unstructured":"Zong, X., and Nephew, K.P. (2019). Ovarian Cancer Stem Cells: Role in Metastasis and Opportunity for Therapeutic Targeting. Cancers, 11.","DOI":"10.3390\/cancers11070934"},{"key":"ref_96","doi-asserted-by":"crossref","unstructured":"Walcher, L., Kistenmacher, A.-K., Suo, H., Kitte, R., Dluczek, S., Strau\u00df, A., Blaudszun, A.-R., Yevsa, T., Fricke, S., and Kossatz-Boehlert, U. (2020). Cancer Stem Cells\u2014Origins and Biomarkers: Perspectives for Targeted Personalized Therapies. Front. Immunol., 11.","DOI":"10.3389\/fimmu.2020.01280"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1186\/s12943-017-0638-3","article-title":"Ovarian cancer stem cells: Still an elusive entity?","volume":"16","author":"Lupia","year":"2017","journal-title":"Mol. Cancer"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.devcel.2021.12.007","article-title":"Quiescent human glioblastoma cancer stem cells drive tumor initiation, expansion, and recurrence following chemotherapy","volume":"57","author":"Xie","year":"2022","journal-title":"Dev. Cell"},{"key":"ref_99","doi-asserted-by":"crossref","unstructured":"Sistigu, A., Musella, M., Galassi, C., Vitale, I., and De Maria, R. (2020). Tuning Cancer Fate: Tumor Microenvironment\u2019s Role in Cancer Stem Cell Quiescence and Reawakening. Front. Immunol., 11.","DOI":"10.3389\/fimmu.2020.02166"},{"key":"ref_100","doi-asserted-by":"crossref","unstructured":"Chan, I.S., Kn\u00fatsd\u00f3ttir, H., Ramakrishnan, G., Padmanaban, V., Warrier, M., Ramirez, J.C., Dunworth, M., Zhang, H., Jaffee, E.M., and Bader, J.S. (2020). Cancer cells educate natural killer cells to a metastasis-promoting cell state. J. Cell Biol., 219.","DOI":"10.1083\/jcb.202001134"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"4725","DOI":"10.1073\/pnas.1424795112","article-title":"CD14-expressing cancer cells establish the inflammatory and proliferative tumor microenvironment in bladder cancer","volume":"112","author":"Cheah","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"5021","DOI":"10.1158\/0008-5472.CAN-20-3251","article-title":"The CD200\u2013CD200R Axis Promotes Squamous Cell Carcinoma Metastasis via Regulation of Cathepsin K","volume":"81","author":"Khan","year":"2021","journal-title":"Cancer Res."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"5095","DOI":"10.1172\/JCI99673","article-title":"\u0394Np63-driven recruitment of myeloid-derived suppressor cells promotes metastasis in triple-negative breast cancer","volume":"128","author":"Kumar","year":"2018","journal-title":"J. Clin. Investig."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"e007670","DOI":"10.1136\/jitc-2023-007670","article-title":"M1 macrophages induce PD-L1(hi) cell-led collective invasion in HPV-positive head and neck squamous cell carcinoma via TNF-\u03b1\/CDK4\/UPS14","volume":"11","author":"Wu","year":"2023","journal-title":"J. Immunother. Cancer"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1038\/s43018-020-0068-9","article-title":"Resistance to natural killer cell immunosurveillance confers a selective advantage to polyclonal metastasis","volume":"1","author":"Lo","year":"2020","journal-title":"Nat. Cancer"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/19\/10554\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:07:47Z","timestamp":1760112467000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/19\/10554"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,30]]},"references-count":105,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2024,10]]}},"alternative-id":["ijms251910554"],"URL":"https:\/\/doi.org\/10.3390\/ijms251910554","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,30]]}}}