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The substrate and mechanism of action of many granzymes are unknown, although they diverge among the family members. In this study, we show that mouse CD8+ tumor-infiltrating lymphocytes (TILs) express a unique array of granzymes relative to CD8 T cells outside the tumor microenvironment in multiple tumor models. Granzyme F was one of the most highly upregulated genes in TILs and was exclusively detected in PD1\/TIM3 double-positive CD8 TILs. To determine the function of granzyme F and to improve the cytotoxic response to leukemia, we constructed chimeric Ag receptor T cells to overexpress a single granzyme, granzyme F or the better-characterized granzyme A or B. Using these doubly recombinant T cells, we demonstrated that granzyme F expression improved T cell\u2013mediated cytotoxicity against target leukemia cells and induced a form of cell death other than chimeric Ag receptor T cells expressing only endogenous granzymes or exogenous granzyme A or B. However, increasing expression of granzyme F also had a detrimental impact on the viability of the host T cells, decreasing their persistence in circulation in vivo. These results suggest a unique role for granzyme F as a marker of terminally differentiated CD8 T cells with increased cytotoxicity, but also increased self-directed cytotoxicity, suggesting a potential mechanism for the end of the terminal exhaustion pathway.<\/jats:p>","DOI":"10.4049\/jimmunol.2300334","type":"journal-article","created":{"date-parts":[[2024,2,28]],"date-time":"2024-02-28T14:40:06Z","timestamp":1709131206000},"page":"1381-1391","source":"Crossref","is-referenced-by-count":8,"title":["Granzyme F: Exhaustion Marker and Modulator of Chimeric Antigen Receptor T Cell\u2013Mediated Cytotoxicity"],"prefix":"10.1093","volume":"212","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6503-0647","authenticated-orcid":false,"given":"Zachary L Z","family":"Hay","sequence":"first","affiliation":[{"name":"Department of Immunology and Microbiology, University of Colorado School of Medicine , Aurora, 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CO"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0796-9346","authenticated-orcid":false,"given":"Faye A","family":"Camp","sequence":"additional","affiliation":[{"name":"Department of Immunology and Microbiology, University of Colorado School of Medicine , Aurora, CO"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1498-1925","authenticated-orcid":false,"given":"Mayumi","family":"Fujita","sequence":"additional","affiliation":[{"name":"Department of Immunology and Microbiology, University of Colorado School of Medicine , Aurora, CO"},{"name":"Department of Dermatology, University of Colorado Anschutz Medical Campus , Aurora, CO"},{"name":"Department of Veterans Affairs Medical Center, Veterans Affairs Eastern Colorado Health Care System , Aurora, CO"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8695-7361","authenticated-orcid":false,"given":"Xiao-Jing","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Dermatology, University of Colorado Anschutz Medical Campus , Aurora, CO"},{"name":"Department of Veterans Affairs Medical Center, Veterans Affairs Eastern Colorado Health Care System , Aurora, CO"},{"name":"Department of Pathology, University of Colorado School of Medicine , Aurora, CO"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4776-2622","authenticated-orcid":false,"given":"Brian P","family":"O\u2019Connor","sequence":"additional","affiliation":[{"name":"Center for Genes, Environment and Health, National Jewish Health , Denver, CO"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3820-1724","authenticated-orcid":false,"given":"Jill 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