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Due to its rarity, current knowledge about this tumor is mostly based on single\u2010case reports. The tumor\u2010cell\u2010origin and molecular pathogenesis remain unclear, although the presence of BRAF<\/jats:italic> mutations in some cases suggest it may evolve from papillary thyroid carcinoma (PTC). Here we provide direct evidence of derivation of SCC of the thyroid from PTC, based on a unique combination of likely pathogenic mutations in KEAP1<\/jats:italic>, STK11<\/jats:italic> (LKB1<\/jats:italic>), and RB1<\/jats:italic> found in both tumor components, along with loss of one copy of chromosome 11 and additional somatic mutations in the SCC tumor. Transdifferentiation from PTC to SCC was also evident by immunohistochemistry. Out of eight attempted patient\u2010derived xenografts (PDX) from advanced thyroid cancers, only one derived from thyroid SCC successfully engrafted in immunodeficient NOG mice. Untreated PDXs showed high Ki67 indices but did not reproduce the conspicuous stromal invasion of CDH1low<\/jats:sup>\/SNAI2+<\/jats:sup>\/CDH2+<\/jats:sup> cells that characterized the primary tumor. Based on the mutation profile (NFE2L2<\/jats:italic>, PIK3CA<\/jats:italic>, CDKN2A<\/jats:italic>, and TP53<\/jats:italic>), experiments were designed to evaluate targeted drug therapy using third\u2010passage PDX transplants. The combination of TRK and PI3K inhibitors, cabozantinib and GDC\u20100326, additively reduced PDX growth by nearly 90%. Remarkably, CB\u2010839 (telaglenastat), a glutaminase inhibitor targeting metabolic rewiring downstream of NRF2 activation, was equally effective. Both combined treatment with cabozantinib + GDC\u20100326 and CB\u2010839 monotherapy diminished the expression of NQO1, an NRF2 transcriptional target, in tumor cells. Glutaminase inhibition further promoted squamous differentiation in engrafted tumors. Both investigated SCC tumors were negative for BRAFV600E or any other common driver mutation of thyroid cancer. Collectively, these findings indicate that aberrant activation of the KEAP1\/NRF2 pathway due to somatic mutations is a previously unrecognized feature of thyroid SCC and suggest that glutaminase inhibition may serve as a potential therapeutic option for this subgroup of ATC patients. \u00a9 2025 The Author(s). The Journal of Pathology<\/jats:italic> published by John Wiley & Sons Ltd on behalf of The Pathological Society of Great Britain and Ireland.<\/jats:p>","DOI":"10.1002\/path.6444","type":"journal-article","created":{"date-parts":[[2025,7,2]],"date-time":"2025-07-02T09:51:48Z","timestamp":1751449908000},"page":"481-494","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Involvement of KEAP1<\/scp>\/NRF2<\/scp> pathway in non\u2010BRAF<\/scp> mutated squamous cell carcinoma of the thyroid"],"prefix":"10.1002","volume":"266","author":[{"given":"Elin","family":"Schoultz","sequence":"first","affiliation":[{"name":"Sahlgrenska Center for Cancer Research University of Gothenburg G\u00f6teborg Sweden"},{"name":"Department of Medical Chemistry and Cell Biology, Institute of Biomedicine University of Gothenburg G\u00f6teborg 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