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Metastatic pancreatic neuroendocrine tumours (PanNETs) in particular may progress from a low\/intermediate to a high\u2010grade disease. The aim of this work was to understand the molecular mechanisms underlying metastatic progression as well as PanNET transformation from a low\/intermediate to a high\u2010grade disease. We performed multi\u2010omics analysis (genome\/exome sequencing, total RNA\u2010sequencing and methylation array) of 32 longitudinal samples from six patients with metastatic low\/intermediate grade PanNET. The clonal composition of tumour lesions and underlying phylogeny of each patient were determined with bioinformatics analyses. Findings were validated in post\u2010alkylating chemotherapy samples from 24 patients with PanNET using targeted next generation sequencing. We validate the current PanNET evolutionary model with\n                    <jats:italic>MEN1<\/jats:italic>\n                    inactivation that occurs very early in tumourigenesis. This was followed by pronounced genetic diversity on both spatial and temporal levels, with parallel and convergent tumour evolution involving the ATRX\/DAXX and mechanistic target of the rapamycin (mTOR) pathways. Following alkylating chemotherapy treatment, some PanNETs developed mismatch repair deficiency and acquired a hypermutational phenotype. This was validated among 16 patients with PanNET who had high\u2010grade progression after alkylating chemotherapy, of whom eight had a tumour mutational burden &gt;50 (50%). In comparison, among the eight patients who did not show high\u2010grade progression, 0 had a tumour mutational burden &gt;50 (0%; odds ratio \u2018infinite\u2019, 95% confidence interval 1.8 to \u2018infinite\u2019,\n                    <jats:italic>p<\/jats:italic>\n                    \u2009=\u20090.02). Our findings contribute to broaden the understanding of metastatic\/high\u2010grade PanNETs and suggests that therapy driven disease evolution is an important hallmark of this disease. \u00a9 2024 The Author(s).\n                    <jats:italic>The Journal of Pathology<\/jats:italic>\n                    published by John Wiley &amp; Sons Ltd on behalf of The Pathological Society of Great Britain and Ireland. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.\n                  <\/jats:p>","DOI":"10.1002\/path.6348","type":"journal-article","created":{"date-parts":[[2024,10,3]],"date-time":"2024-10-03T04:25:26Z","timestamp":1727929526000},"page":"357-370","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["The evolutionary history of metastatic pancreatic neuroendocrine tumours reveals a therapy driven route to high\u2010grade transformation"],"prefix":"10.1002","volume":"264","author":[{"given":"Samuel","family":"Backman","sequence":"first","affiliation":[{"name":"Department of Surgical Sciences Uppsala University  Uppsala Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johan","family":"Botling","sequence":"additional","affiliation":[{"name":"Department of Immunology, Genetics and Pathology and Science for Life Laboratory Uppsala University  Uppsala Sweden"},{"name":"Department of Laboratory Medicine, Institute of Biomedicine University of Gothenburg  Gothenburg Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helena","family":"Nord","sequence":"additional","affiliation":[{"name":"Department of Immunology, Genetics and Pathology and Science for Life Laboratory Uppsala University  Uppsala Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Suman","family":"Ghosal","sequence":"additional","affiliation":[{"name":"Section on Medical Neuroendocrinology Eunice Kennedy Shriver National Institute of Child Health and Human Development  Bethesda MD USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"St\u00e5lberg","sequence":"additional","affiliation":[{"name":"Department of Surgical Sciences Uppsala University  Uppsala Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5945-9081","authenticated-orcid":false,"given":"C. 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