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Following transplant, the thymus plays a key role in immune reconstitution by generating a naive \u03b1\u03b2T cell pool from transplant-derived progenitors. While donor-derived thymopoiesis during the early post-transplant period is well studied, the ability of the thymus to synchronize T cell development with essential tolerance mechanisms is poorly understood. Using a syngeneic mouse transplant model, we analyzed T cell recovery alongside the regeneration and function of intrathymic microenvironments. We report a specific and prolonged failure in the post-transplant recovery of medullary thymic epithelial cells (mTECs). This manifests as loss of medulla-dependent tolerance mechanisms, including failures in Foxp3+ regulatory T cell development and formation of the intrathymic dendritic cell pool. In addition, defective negative selection enables escape of self-reactive conventional \u03b1\u03b2T cells that promote autoimmunity. Collectively, we show that post-transplant T cell recovery involves an uncoupling of thymopoiesis from thymic tolerance, which results in autoimmune reconstitution caused by failures in thymic medulla regeneration.<\/jats:p>","DOI":"10.1084\/jem.20211239","type":"journal-article","created":{"date-parts":[[2021,11,18]],"date-time":"2021-11-18T02:21:54Z","timestamp":1637202114000},"update-policy":"https:\/\/doi.org\/10.1084\/jem.crossmarkpolicy","source":"Crossref","is-referenced-by-count":31,"title":["Failures in thymus medulla regeneration during immune recovery cause tolerance loss and prime recipients for auto-GVHD"],"prefix":"10.1084","volume":"219","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4844-1801","authenticated-orcid":true,"given":"Abdullah S.","family":"Alawam","sequence":"first","affiliation":[{"name":"Institute for Immunology and Immunotherapy, College of Medical and Dental Sciences, Medical School, University of Birmingham, Birmingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7207-2511","authenticated-orcid":true,"given":"Emilie J.","family":"Cosway","sequence":"additional","affiliation":[{"name":"Institute for Immunology and Immunotherapy, College of Medical and Dental Sciences, Medical School, University of Birmingham, Birmingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8811-6996","authenticated-orcid":true,"given":"Kieran D.","family":"James","sequence":"additional","affiliation":[{"name":"Institute for Immunology and Immunotherapy, College of Medical and Dental Sciences, Medical School, University of Birmingham, Birmingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2947-5432","authenticated-orcid":true,"given":"Beth","family":"Lucas","sequence":"additional","affiliation":[{"name":"Institute for Immunology and Immunotherapy, College of Medical and Dental Sciences, Medical School, University of Birmingham, Birmingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2688-8952","authenticated-orcid":true,"given":"Andrea","family":"Bacon","sequence":"additional","affiliation":[{"name":"Institute for Immunology and Immunotherapy, College of Medical and Dental Sciences, Medical School, University of Birmingham, Birmingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4430-9072","authenticated-orcid":true,"given":"Sonia M.","family":"Parnell","sequence":"additional","affiliation":[{"name":"Institute for Immunology and Immunotherapy, College of Medical and Dental Sciences, Medical School, University of Birmingham, Birmingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6950-6729","authenticated-orcid":true,"given":"Andrea J.","family":"White","sequence":"additional","affiliation":[{"name":"Institute for Immunology and Immunotherapy, College of Medical and Dental Sciences, Medical School, University of Birmingham, Birmingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3422-8372","authenticated-orcid":true,"given":"William E.","family":"Jenkinson","sequence":"additional","affiliation":[{"name":"Institute for Immunology and Immunotherapy, College of Medical and Dental Sciences, Medical School, University of Birmingham, Birmingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2917-4085","authenticated-orcid":true,"given":"Graham","family":"Anderson","sequence":"additional","affiliation":[{"name":"Institute for Immunology and Immunotherapy, College of Medical and Dental Sciences, Medical School, University of Birmingham, Birmingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"291","published-online":{"date-parts":[[2021,12,15]]},"reference":[{"key":"2023072616420815500_bib1","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1053\/j.seminhematol.2013.03.026","article-title":"Mouse models in bone marrow transplantation and adoptive cellular therapy","volume":"50","author":"Arber","year":"2013","journal-title":"Semin. 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