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The distribution of oligodendroglioma age is non-Gaussian and reportedly bimodal, which motivated our investigation of age-associated molecular alterations that may drive poorer outcomes. We found that elevated HOXD12 expression was associated with both older patient age and shorter survival in the TCGA (FDR\u2009&lt;\u20090.01, FDR\u2009=\u20091e\u22125) and the CGGA (<jats:italic>p<\/jats:italic>\u2009=\u20090.03, <jats:italic>p<\/jats:italic>\u2009&lt;\u20091e\u22123). <jats:italic>HOXD12<\/jats:italic> gene body hypermethylation was associated with older age, higher WHO grade, and shorter survival in the TCGA (<jats:italic>p<\/jats:italic>\u2009&lt;\u20091e\u22126, <jats:italic>p<\/jats:italic>\u2009&lt;\u20090.001, <jats:italic>p<\/jats:italic>\u2009&lt;\u20091e\u22123) and with older age and higher WHO grade in Capper et al. (<jats:italic>p<\/jats:italic>\u2009&lt;\u20090.002, <jats:italic>p<\/jats:italic>\u2009=\u20090.014). In the TCGA, <jats:italic>HOXD12<\/jats:italic> gene body hypermethylation and elevated expression were independently prognostic of <jats:italic>NOTCH1<\/jats:italic> and <jats:italic>PIK3CA<\/jats:italic> mutations, loss of 15q, MYC activation, and standard histopathological features. Single-nucleus RNA and ATAC sequencing data showed that HOXD12 activity was elevated in neoplastic tissue, particularly within cycling and OPC-like cells, and was associated with a stem-like phenotype. A pan-HOX DNA methylation analysis revealed an age and survival-associated HOX-high signature that was tightly associated with <jats:italic>HOXD12<\/jats:italic> gene body methylation. Overall, HOXD12 expression and gene body hypermethylation were associated with an older, atypically aggressive subtype of oligodendroglioma.<\/jats:p>","DOI":"10.1007\/s00401-024-02802-1","type":"journal-article","created":{"date-parts":[[2024,9,11]],"date-time":"2024-09-11T11:09:18Z","timestamp":1726052958000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["HOXD12 defines an age-related aggressive subtype of oligodendroglioma"],"prefix":"10.1007","volume":"148","author":[{"given":"Nicholas","family":"Nuechterlein","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sadie","family":"Cimino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Allison","family":"Shelbourn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vinny","family":"Ha","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sonali","family":"Arora","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sharika","family":"Rajan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linda G.","family":"Shapiro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric C.","family":"Holland","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kenneth","family":"Aldape","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tresa","family":"McGranahan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark R.","family":"Gilbert","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0441-4502","authenticated-orcid":false,"given":"Patrick J.","family":"Cimino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,9,11]]},"reference":[{"key":"2802_CR1","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1002\/path.1939","volume":"209","author":"R Abdel-Fattah","year":"2006","unstructured":"Abdel-Fattah R, Xiao A, Bomgardner D, Pease CS, Lopes MB, Hussaini IM (2006) Differential expression of HOX genes in neoplastic and non-neoplastic human astrocytes. 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