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Spatial genome organization plays a crucial role in oncogenic transformation and progression, but the extent to which chromosome architecture contributes to organ-specific metastatic traits is unclear. This work characterizes chromosome architecture changes associated with organotropic metastatic traits. By comparing a collection of human genomic data from different subtypes of localized and lung metastatic breast cancer cells with both normal and cancerous lung cells, we find important trends of genomic reorganization. The most striking differences in 3D genome compartments segregate cell types according to their epithelial vs. mesenchymal status. This epithelial\u2013mesenchymal transition (EMT) compartment signature occurs at genomic regions distinct from transcription-defined EMT signatures, suggesting a separate layer of regulation. Specifically querying organotropism, we find 3D genome changes consistent with adaptations needed to survive in a new microenvironment, with lung metastatic breast cancer cells exhibiting compartment switch signatures that shift the genome architecture to a lung cell-like conformation and brain metastatic prostate cancer cells showing compartment shifts toward a brain-like state. TCGA patient data reveals gene expression changes concordant with these organ-permissive compartment changes. These results suggest that genome architecture provides an additional level of cell fate specification informing organotropism and enabling survival at the metastatic site.<\/jats:p>","DOI":"10.7554\/elife.103697","type":"journal-article","created":{"date-parts":[[2024,12,23]],"date-time":"2024-12-23T09:25:10Z","timestamp":1734945910000},"update-policy":"https:\/\/doi.org\/10.7554\/elife.103697","source":"Crossref","is-referenced-by-count":1,"title":["Rearrangement of 3D genome organization in breast cancer epithelial to mesenchymal transition and metastasis organotropism"],"prefix":"10.7554","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6774-6718","authenticated-orcid":true,"given":"Priyojit","family":"Das","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/020f3ap87","id-type":"ROR","asserted-by":"publisher"}],"name":"UT-ORNL Graduate School of Genome Science and Technology, University of Tennessee","place":["Knoxville, United States"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"conceptualization","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7249-3922","authenticated-orcid":true,"given":"Rebeca","family":"San Martin","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/020f3ap87","id-type":"ROR","asserted-by":"publisher"}],"name":"Biochemistry & Cellular and Molecular Biology, University of Tennessee","place":["Knoxville, United States"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"conceptualization","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8212-7050","authenticated-orcid":true,"given":"Tian","family":"Hong","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/020f3ap87","id-type":"ROR","asserted-by":"publisher"}],"name":"UT-ORNL Graduate School of Genome Science and Technology, University of Tennessee","place":["Knoxville, United States"]},{"id":[{"id":"https:\/\/ror.org\/020f3ap87","id-type":"ROR","asserted-by":"publisher"}],"name":"Biochemistry & Cellular and Molecular Biology, University of Tennessee","place":["Knoxville, United States"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"data-curation","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0010-5323","authenticated-orcid":true,"given":"Rachel Patton","family":"McCord","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/020f3ap87","id-type":"ROR","asserted-by":"publisher"}],"name":"UT-ORNL Graduate School of Genome Science and Technology, University of Tennessee","place":["Knoxville, United States"]},{"id":[{"id":"https:\/\/ror.org\/020f3ap87","id-type":"ROR","asserted-by":"publisher"}],"name":"Biochemistry & Cellular and Molecular Biology, University of Tennessee","place":["Knoxville, United States"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"corresponding-author","vocabulary":"crossref"},{"role":"conceptualization","vocabulary":"credit"},{"role":"funding-acquisition","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"}]}],"member":"4374","published-online":{"date-parts":[[2025,11,12]]},"reference":[{"key":"bib1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-14098-x","type":"journal-article","article-title":"Epigenetic reprogramming at estrogen-receptor binding sites alters 3D chromatin landscape in endocrine-resistant breast cancer","volume":"11","author":"Achinger-Kawecka","year":"2020","journal-title":"Nature Communications"},{"key":"bib2","doi-asserted-by":"publisher","first-page":"166","DOI":"10.1093\/bioinformatics\/btu638","type":"journal-article","article-title":"HTSeq--a Python framework to work with high-throughput sequencing data","volume":"31","author":"Anders","year":"2015","journal-title":"Bioinformatics"},{"key":"bib3","type":"software","article-title":"HTSeq","volume-title":"GitHub","author":"Anders","year":"2020","unstructured":"Anders S, Zanini Z. 2020. 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