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Following CAR T-cell infusion, 1 patient developed a gradually enlarging retroperitoneal tumor due to a CAR-expressing CD4+ T-cell lymphoma. Screening of other patients led to the detection, in an asymptomatic patient, of a second CAR T-cell tumor in thoracic para-aortic lymph nodes. Analysis of the first lymphoma showed a high transgene copy number, but no insertion into typical oncogenes. There were also structural changes such as altered genomic copy number and point mutations unrelated to the insertion sites. Transcriptome analysis showed transgene promoter\u2013driven upregulation of transcription of surrounding regions despite insulator sequences surrounding the transgene. However, marked global changes in transcription predominantly correlated with gene copy number rather than insertion sites. In both patients, the CAR T-cell\u2013derived lymphoma progressed and 1 patient died. We describe the first 2 cases of malignant lymphoma derived from CAR gene\u2013modified T cells. Although CAR T cells have an enviable record of safety to date, our results emphasize the need for caution and regular follow-up of CAR T recipients, especially when novel methods of gene transfer are used to create genetically modified immune therapies. This trial was registered at www.anzctr.org.au as ACTRN12617001579381.<\/jats:p>","DOI":"10.1182\/blood.2021010858","type":"journal-article","created":{"date-parts":[[2021,5,11]],"date-time":"2021-05-11T16:41:41Z","timestamp":1620751301000},"page":"1391-1405","update-policy":"https:\/\/doi.org\/10.1182\/blood.2019cm0000","source":"Crossref","is-referenced-by-count":232,"title":["Investigation of product-derived lymphoma following infusion of <i>piggyBac<\/i>-modified CD19 chimeric antigen receptor T cells"],"prefix":"10.1182","volume":"138","author":[{"given":"Kenneth P.","family":"Micklethwaite","sequence":"first","affiliation":[{"name":"Blood Transplant and Cell Therapies Program, Department of Haematology, Westmead Hospital, Sydney, NSW, Australia;"},{"name":"Blood Transplant and Cell Therapies Laboratory, NSW Health Pathology\u2013ICPMR Westmead, Sydney, NSW, Australia;"},{"name":"Sydney Medical School, Faculty of Medicine and Health, University of Sydney, Sydney, NSW, Australia;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kavitha","family":"Gowrishankar","sequence":"additional","affiliation":[{"name":"Westmead Institute for Medical Research, Sydney, NSW, Australia;"},{"name":"Sydney Medical School, Faculty of Medicine and Health, University of Sydney, Sydney, NSW, Australia;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brian S.","family":"Gloss","sequence":"additional","affiliation":[{"name":"Westmead Institute for Medical Research, Sydney, NSW, Australia;"},{"name":"Sydney Medical School, Faculty of Medicine and Health, University of Sydney, Sydney, NSW, Australia;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ziduo","family":"Li","sequence":"additional","affiliation":[{"name":"Westmead Institute for Medical Research, Sydney, NSW, Australia;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janine A.","family":"Street","sequence":"additional","affiliation":[{"name":"Westmead Institute for Medical Research, Sydney, NSW, Australia;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leili","family":"Moezzi","sequence":"additional","affiliation":[{"name":"Westmead Institute for Medical Research, Sydney, NSW, Australia;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melanie A.","family":"Mach","sequence":"additional","affiliation":[{"name":"Westmead Institute for Medical Research, Sydney, NSW, Australia;"},{"name":"Sydney Medical School, Faculty of Medicine and Health, University of Sydney, Sydney, NSW, Australia;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gaurav","family":"Sutrave","sequence":"additional","affiliation":[{"name":"Blood Transplant and Cell Therapies Program, Department of Haematology, Westmead Hospital, Sydney, NSW, Australia;"},{"name":"Westmead Institute for Medical Research, Sydney, NSW, Australia;"},{"name":"Sydney Medical School, Faculty of Medicine and Health, University of Sydney, Sydney, NSW, Australia;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leighton E.","family":"Clancy","sequence":"additional","affiliation":[{"name":"Blood Transplant and Cell Therapies Laboratory, NSW Health Pathology\u2013ICPMR Westmead, Sydney, NSW, Australia;"},{"name":"Westmead Institute for Medical Research, Sydney, NSW, Australia;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David C.","family":"Bishop","sequence":"additional","affiliation":[{"name":"Blood Transplant and Cell Therapies Program, Department of Haematology, Westmead Hospital, Sydney, NSW, Australia;"},{"name":"Westmead Institute for Medical Research, Sydney, NSW, Australia;"},{"name":"Sydney Medical School, Faculty of Medicine and Health, University of Sydney, Sydney, NSW, Australia;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9384-2447","authenticated-orcid":false,"given":"Raymond H. 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