{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,26]],"date-time":"2026-06-26T18:54:38Z","timestamp":1782500078724,"version":"3.54.5"},"reference-count":31,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,10,9]],"date-time":"2024-10-09T00:00:00Z","timestamp":1728432000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"},{"start":{"date-parts":[[2024,10,9]],"date-time":"2024-10-09T00:00:00Z","timestamp":1728432000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["1903346"],"award-info":[{"award-number":["1903346"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["1903346"],"award-info":[{"award-number":["1903346"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["2303926"],"award-info":[{"award-number":["2303926"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"DOI":"10.1038\/s41598-024-73688-y","type":"journal-article","created":{"date-parts":[[2024,10,9]],"date-time":"2024-10-09T12:02:47Z","timestamp":1728475367000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Three-dimensional computer vision for exploring heterogeneity in collective Cancer Invasion"],"prefix":"10.1038","volume":"14","author":[{"given":"Yanlin","family":"Li","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ninghao","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mona","family":"Ahmed","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julio","family":"Urbina","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tai-Yin","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pak Kin","family":"Wong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,10,9]]},"reference":[{"key":"73688_CR1","doi-asserted-by":"publisher","first-page":"1559","DOI":"10.1126\/science.1203543","volume":"331","author":"CL Chaffer","year":"2011","unstructured":"Chaffer, C. L. & Weinberg, R. A. A perspective on cancer cell metastasis. Science. 331, 1559\u20131564 (2011).","journal-title":"Science"},{"key":"73688_CR2","doi-asserted-by":"publisher","first-page":"777","DOI":"10.1038\/ncb2548","volume":"14","author":"P Friedl","year":"2012","unstructured":"Friedl, P., Locker, J., Sahai, E. & Segall, J. E. Classifying collective cancer cell invasion. Nat. cell. Biology. 14, 777\u2013783 (2012).","journal-title":"Nat. cell. Biology"},{"key":"73688_CR3","doi-asserted-by":"publisher","first-page":"592","DOI":"10.1038\/s41568-021-00376-8","volume":"21","author":"SA Vilchez Mercedes","year":"2021","unstructured":"Vilchez Mercedes, S. A. et al. Decoding leader cells in collective cancer invasion. Nat. Rev. Cancer. 21, 592\u2013604 (2021).","journal-title":"Nat. Rev. Cancer"},{"key":"73688_CR4","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1038\/s41580-022-00530-6","volume":"24","author":"S Linder","year":"2023","unstructured":"Linder, S., Cervero, P., Eddy, R. & Condeelis, J. Mechanisms and roles of podosomes and invadopodia. Nat. Rev. Mol. Cell. Biol. 24, 86\u2013106 (2023).","journal-title":"Nat. Rev. Mol. Cell. Biol."},{"key":"73688_CR5","doi-asserted-by":"publisher","first-page":"736","DOI":"10.1016\/j.tcb.2011.09.006","volume":"21","author":"K Wolf","year":"2011","unstructured":"Wolf, K. & Friedl, P. Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell. Biology. 21, 736\u2013744 (2011).","journal-title":"Trends cell. Biology"},{"key":"73688_CR6","doi-asserted-by":"publisher","first-page":"jcs231514","DOI":"10.1242\/jcs.231514","volume":"132","author":"EL Zoeller","year":"2019","unstructured":"Zoeller, E. L. et al. Genetic heterogeneity within collective invasion packs drives leader and follower cell phenotypes. J. Cell. Sci. 132, jcs231514 (2019).","journal-title":"J. cell. Sci."},{"key":"73688_CR7","doi-asserted-by":"publisher","first-page":"1927","DOI":"10.1172\/JCI77767","volume":"125","author":"JM Westcott","year":"2015","unstructured":"Westcott, J. M. et al. An epigenetically distinct breast cancer cell subpopulation promotes collective invasion. J. Clin. Invest. 125, 1927\u20131943 (2015).","journal-title":"J. Clin. Invest."},{"key":"73688_CR8","first-page":"5301","volume":"11","author":"Y Yang","year":"2019","unstructured":"Yang, Y., Zheng, H., Zhan, Y. & Fan, S. An emerging tumor invasion mechanism about the collective cell migration. Am. J. Transl Res. 11, 5301\u20135312 (2019).","journal-title":"Am. J. Transl Res."},{"key":"73688_CR9","doi-asserted-by":"publisher","first-page":"100310","DOI":"10.1016\/j.cobme.2021.100310","volume":"19","author":"DS Shin","year":"2021","unstructured":"Shin, D. S. & Anseth, K. S. Recent advances in 3d models of tumor invasion. Curr. Opin. Biomedical Eng. 19, 100310 (2021).","journal-title":"Curr. Opin. Biomedical Eng."},{"key":"73688_CR10","doi-asserted-by":"publisher","first-page":"3084","DOI":"10.3390\/cells10113084","volume":"10","author":"P Torab","year":"2021","unstructured":"Torab, P. et al. Intratumoral heterogeneity promotes collective cancer invasion through notch1 variation. Cells. 10, 3084 (2021).","journal-title":"Cells"},{"key":"73688_CR11","doi-asserted-by":"publisher","first-page":"8768","DOI":"10.1021\/acs.analchem.0c00057","volume":"92","author":"P Torab","year":"2020","unstructured":"Torab, P. et al. Three-dimensional microtumors for probing heterogeneity of invasive bladder cancer. Anal. Chem. 92, 8768\u20138775 (2020).","journal-title":"Anal. Chem."},{"key":"73688_CR12","doi-asserted-by":"publisher","first-page":"27423","DOI":"10.1073\/pnas.2010872117","volume":"117","author":"G Chrisafis","year":"2020","unstructured":"Chrisafis, G. et al. Collective cancer cell invasion requires rna accumulation at the invasive front. Proc. Natl. Acad. Sci. 117, 27423\u201327434 (2020).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"73688_CR13","doi-asserted-by":"publisher","first-page":"722","DOI":"10.1039\/D1AN01802G","volume":"147","author":"SAV Mercedes","year":"2022","unstructured":"Mercedes, S. A. V., Eder, I., Ahmed, M., Zhu, N. & Wong, P. K. Optimizing locked nucleic acid modification in double-stranded biosensors for live single cell analysis. Analyst. 147, 722\u2013733 (2022).","journal-title":"Analyst"},{"key":"73688_CR14","doi-asserted-by":"crossref","unstructured":"Zhu, N., Ahmed, M., Li, Y., Liao, J. C. & Wong, P. K. Long noncoding rna malat1 is dynamically regulated in leader cells during collective cancer invasion. Proc. Natl. Acad. Sci. 120, e2305410120 (2023).","DOI":"10.1073\/pnas.2305410120"},{"key":"73688_CR15","doi-asserted-by":"publisher","first-page":"8902","DOI":"10.1021\/acs.analchem.6b02608","volume":"88","author":"ZS Dean","year":"2016","unstructured":"Dean, Z. S., Elias, P., Jamilpour, N., Utzinger, U. & Wong, P. K. Probing 3d collective cancer invasion using double-stranded locked nucleic acid biosensors. Anal. Chem. 88, 8902\u20138907 (2016).","journal-title":"Anal. Chem."},{"key":"73688_CR16","doi-asserted-by":"publisher","first-page":"eabl8876","DOI":"10.1126\/science.abl8876","volume":"375","author":"K Kozyrska","year":"2022","unstructured":"Kozyrska, K. et al. p53 directs leader cell behavior, migration, and clearance during epithelial repair. Science. 375, eabl8876 (2022).","journal-title":"Science"},{"key":"73688_CR17","doi-asserted-by":"publisher","first-page":"6556","DOI":"10.1038\/ncomms7556","volume":"6","author":"R Riahi","year":"2015","unstructured":"Riahi, R. et al. Notch1\u2013dll4 signalling and mechanical force regulate leader cell formation during collective cell migration. Nat. Commun. 6, 6556 (2015).","journal-title":"Nat. Commun."},{"key":"73688_CR18","doi-asserted-by":"publisher","first-page":"807324","DOI":"10.3389\/fmolb.2022.807324","volume":"9","author":"SA Vilchez Mercedes","year":"2022","unstructured":"Vilchez Mercedes, S. A. et al. Nrf2 modulates the hybrid epithelial\/mesenchymal phenotype and notch signaling during collective cancer migration. Front. Mol. Biosci. 9, 807324 (2022).","journal-title":"Front. Mol. Biosci."},{"key":"73688_CR19","doi-asserted-by":"publisher","first-page":"1639","DOI":"10.1016\/j.cell.2013.11.029","volume":"155","author":"KJ Cheung","year":"2013","unstructured":"Cheung, K. J., Gabrielson, E., Werb, Z. & Ewald, A. J. Collective invasion in breast cancer requires a conserved basal epithelial program. Cell. 155, 1639\u20131651 (2013).","journal-title":"Cell"},{"key":"73688_CR20","doi-asserted-by":"publisher","first-page":"eaaz6197","DOI":"10.1126\/sciadv.aaz6197","volume":"6","author":"ER Summerbell","year":"2020","unstructured":"Summerbell, E. R. et al. Epigenetically heterogeneous tumor cells direct collective invasion through filopodia-driven fibronectin micropatterning. Sci. Adv. 6, eaaz6197 (2020).","journal-title":"Sci. Adv."},{"key":"73688_CR21","first-page":"615","volume":"24","author":"TH Booij","year":"2019","unstructured":"Booij, T. H., Price, L. S. & Danen, E. H. 3d cell-based assays for drug screens: challenges in imaging, image analysis, and high-content analysis. SLAS Discov Adv. Life Sci. R&D. 24, 615\u2013627 (2019).","journal-title":"SLAS Discov Adv. Life Sci. R&D"},{"key":"73688_CR22","doi-asserted-by":"publisher","first-page":"606","DOI":"10.1038\/nrd.2018.99","volume":"17","author":"N Carragher","year":"2018","unstructured":"Carragher, N. et al. Concerns, challenges and promises of high-content analysis of 3d cellular models. Nat. Reviews Drug Discovery. 17, 606\u2013606 (2018).","journal-title":"Nat. Reviews Drug Discovery"},{"key":"73688_CR23","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1007\/BF01189221","volume":"11","author":"J Serra","year":"1992","unstructured":"Serra, J. & Vincent, L. An overview of morphological filtering. Circuits Syst. Signal. Process. 11, 47\u2013108 (1992).","journal-title":"Circuits Syst. Signal. Process."},{"key":"73688_CR24","doi-asserted-by":"publisher","first-page":"505","DOI":"10.1109\/83.826787","volume":"9","author":"A Polesel","year":"2000","unstructured":"Polesel, A., Ramponi, G. & Mathews, V. J. Image enhancement via adaptive unsharp masking. IEEE Trans. Image Process. 9, 505\u2013510 (2000).","journal-title":"IEEE Trans. Image Process."},{"key":"73688_CR25","doi-asserted-by":"crossref","unstructured":"Vincent, L. Morphological area openings and closings for grey-scale images. In Shape in Picture: Mathematical Description of Shape in Grey-Level Images, 197\u2013208 (Springer, 1994).","DOI":"10.1007\/978-3-662-03039-4_13"},{"key":"73688_CR26","doi-asserted-by":"publisher","first-page":"4051","DOI":"10.3390\/rs15164051","volume":"15","author":"Y Li","year":"2023","unstructured":"Li, Y., Galindo, F., Urbina, J., Zhou, Q. & Huang T.-Y. A machine learning algorithm to detect and analyze meteor echoes observed by the Jicamarca radar. Remote Sens. 15, 4051 (2023).","journal-title":"Remote Sens."},{"key":"73688_CR27","doi-asserted-by":"crossref","unstructured":"Haralick, R. M., Sternberg, S. R. & Zhuang, X. Image analysis using mathematical morphology. IEEE Trans. Pattern Anal. Mach. Intell. 532\u2013550 (1987).","DOI":"10.1109\/TPAMI.1987.4767941"},{"key":"73688_CR28","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1109\/TIP.2008.2007067","volume":"18","author":"CC Cheng","year":"2008","unstructured":"Cheng, C. C., Peng, G. J. & Hwang, W. L. Subband weighting with pixel connectivity for 3-d wavelet coding. IEEE Trans. Image Process. 18, 52\u201362 (2008).","journal-title":"IEEE Trans. Image Process."},{"key":"73688_CR29","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1007\/s13735-020-00195-x","volume":"9","author":"AM Hafiz","year":"2020","unstructured":"Hafiz, A. M. & Bhat, G. M. A survey on instance segmentation: state of the art. Int. J. Multimedia Inform. Retr. 9, 171\u2013189 (2020).","journal-title":"Int. J. Multimedia Inform. Retr."},{"key":"73688_CR30","doi-asserted-by":"publisher","DOI":"10.6084\/m9.figshare.853801","author":"Z Hao","year":"2014","unstructured":"Hao, Z., AghaKouchak, A., Nakhjiri, N. & Farahmand, A. Global integrated drought monitoring and prediction system (GIDMaPS) data sets. Figshare. https:\/\/doi.org\/10.6084\/m9.Figshare.853801 (2014).","journal-title":"Figshare"},{"key":"73688_CR31","doi-asserted-by":"publisher","DOI":"10.5281\/zenodo.12805016","author":"Y Li","year":"2024","unstructured":"Li, Y. Three-dimensional computer vision for exploring heterogeneity in collective Cancer Invasion. Zenodo. https:\/\/doi.org\/10.5281\/zenodo.12805016 (2024).","journal-title":"Zenodo"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-73688-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-73688-y","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-73688-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,9]],"date-time":"2024-10-09T12:05:55Z","timestamp":1728475555000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-73688-y"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,9]]},"references-count":31,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["73688"],"URL":"https:\/\/doi.org\/10.1038\/s41598-024-73688-y","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10,9]]},"assertion":[{"value":"11 March 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"19 September 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"9 October 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"23560"}}