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We performed an integrative transcriptomic analysis of 1232 PCa samples spanning normal prostate and all major disease stages including primary localized tumors, metastatic hormone-sensitive PCa (mHSPC), and metastatic castration-resistant PCa (mCRPC). By integrating unsupervised consensus clustering (ATC:hclust), weighted gene co-expression network analysis (WGCNA), and explainable machine learning (ML), we identified key transcriptional programs and biomarkers associated with cancer initiation and disease progression. Our analysis revealed persistent dysregulation of mitotic control, DNA damage repair, transcriptional regulation, and cytoskeletal remodeling, underscoring their functional relevance for PCa progression. We uncovered\n                    <jats:italic>TPX2<\/jats:italic>\n                    as a central hub gene, consistently upregulated across all disease stages and co-expressed with 21 commonly upregulated genes. ML-based gene ranking and interaction analysis identified connections among the commonly upregulated genes, highlighting\n                    <jats:italic>CENPA-MYBL2<\/jats:italic>\n                    for primary localized PCa,\n                    <jats:italic>EXO1-NEIL3<\/jats:italic>\n                    for mHSPC and\n                    <jats:italic>CENPA-RRM2<\/jats:italic>\n                    for mCRPC. Stage-specific analysis further identified key drivers of distinct disease transitions including\n                    <jats:italic>EZH2<\/jats:italic>\n                    and\n                    <jats:italic>PLK1<\/jats:italic>\n                    as major regulators of androgen dependence in mHSPC, and\n                    <jats:italic>TERT<\/jats:italic>\n                    as a hallmark of mCRPC, highlighting its role in telomere maintenance and tumor progression. This study demonstrates that unsupervised clustering combined with WGCNA and ML enables the discovery of clinically relevant molecular signatures in PCa. Our findings establish\n                    <jats:italic>TPX2<\/jats:italic>\n                    -centered networks together with biological pathways implicated in mitotic regulation and DNA damage repair as key drivers of tumor evolution, providing a biologically informed source for biomarker development, drug testing and mechanistic studies.\n                  <\/jats:p>","DOI":"10.1038\/s41598-025-27704-4","type":"journal-article","created":{"date-parts":[[2025,12,16]],"date-time":"2025-12-16T10:33:40Z","timestamp":1765881220000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Unravelling TPX2-centered co-expression networks as key drivers of aggressive prostate cancer"],"prefix":"10.1038","volume":"15","author":[{"given":"Raheleh","family":"Sheibani-Tezerji","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carlos Uziel","family":"Perez Malla","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gabriel","family":"Wasinger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katarina","family":"Misura","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Astrid","family":"Haase","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Malzer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jessica","family":"Kalla","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Loan","family":"Tran","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gerda","family":"Egger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,12,16]]},"reference":[{"key":"27704_CR1","doi-asserted-by":"publisher","first-page":"209","DOI":"10.3322\/caac.21660","volume":"71","author":"H Sung","year":"2021","unstructured":"Sung, H. et al. 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