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Although CD4<jats:sup>+<\/jats:sup>CD26<jats:sup>high<\/jats:sup>T cells are considered for adoptive cancer immunotherapy, the role of CD8<jats:sup>+<\/jats:sup>CD26<jats:sup>+<\/jats:sup>T cells is ill-defined. Therefore, further studies are required to better determine the role of CD8<jats:sup>+<\/jats:sup>CD26<jats:sup>+<\/jats:sup>T cells in solid tumors and haematological cancers.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We studied 55 CLL and 44 age-sex-matched healthy controls (HCs). The expression of CD26 on different T cell subsets (e.g. na\u00efve, memory, effector, and etc.) was analyzed. Also, functional properties of CD8<jats:sup>+<\/jats:sup>CD26<jats:sup>+<\/jats:sup>and CD8<jats:sup>+<\/jats:sup>CD26<jats:sup>\u2212<\/jats:sup>T cells were evaluated. Finally, the plasma cytokine\/chemokine and Galectin-9 (Gal-9) levels were examined.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>CD26 expression identifies three CD8<jats:sup>+<\/jats:sup>T cell subsets with distinct immunological properties. While CD26<jats:sup>neg<\/jats:sup>CD8<jats:sup>+<\/jats:sup>T cells are mainly transitional, effector memory and effectors, CD26<jats:sup>low<\/jats:sup>CD8<jats:sup>+<\/jats:sup>T cells are mainly na\u00efve, stem cell, and central memory but CD26<jats:sup>high<\/jats:sup>\u00a0T cells are differentiated to transitional and effector memory. CD26<jats:sup>+<\/jats:sup>CD8<jats:sup>+<\/jats:sup>T cells are significantly reduced in CLL patients versus HCs. CD26<jats:sup>high<\/jats:sup>\u00a0cells are enriched with Mucosal Associated Invariant T (MAIT) cells co-expressing CD161TV\u03b17.2 and IL-18R\u03b1. Also, CD26<jats:sup>high<\/jats:sup>cells have a rich chemokine receptor profile (e.g. CCR5 and CCR6), profound cytokine (TNF-\u03b1, IFN-\u03b3, and IL-2), and cytolytic molecules (Granzyme B, K, and perforin) expression upon stimulation. CD26<jats:sup>high<\/jats:sup>and CD26<jats:sup>low<\/jats:sup>T cells exhibit significantly lower frequencies of CD160, 2B4, TIGIT, ICOS, CD39, and PD-1 but higher levels of CD27, CD28, and CD73 versus CD26<jats:sup>neg<\/jats:sup>cells. To understand the mechanism linked to CD26<jats:sup>high<\/jats:sup>depletion, we found that malignant B cells by shedding Galectin-9 (Gal-9) contribute to the elevation of plasma Gal-9 in CLL patients. In turn, Gal-9 and the inflammatory milieu (IL-18, IL-12, and IL-15) in CLL patients contribute to increased apoptosis of CD26<jats:sup>high<\/jats:sup>T cells.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusions<\/jats:title><jats:p>Our results demonstrate that CD26<jats:sup>+<\/jats:sup>\u00a0T cells possess a natural polyfunctionality to traffic and exhibit effector functions and resist exhaustion. Therefore, they can be proposed for adoptive cancer immunotherapy. Finally, neutralizing and\/or inhibiting Gal-9 may preserve CD26<jats:sup>high<\/jats:sup>CD8<jats:sup>+<\/jats:sup>T cells in CLL.<\/jats:p><\/jats:sec>","DOI":"10.1186\/s40164-023-00375-5","type":"journal-article","created":{"date-parts":[[2023,1,27]],"date-time":"2023-01-27T08:03:37Z","timestamp":1674806617000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":29,"title":["Depletion of polyfunctional CD26highCD8+ T cells repertoire in chronic lymphocytic leukemia"],"prefix":"10.1186","volume":"12","author":[{"given":"Najmeh","family":"Bozorgmehr","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark","family":"Hnatiuk","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anthea C.","family":"Peters","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7215-2009","authenticated-orcid":false,"given":"Shokrollah","family":"Elahi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,1,27]]},"reference":[{"key":"375_CR1","doi-asserted-by":"publisher","first-page":"5063","DOI":"10.1073\/pnas.0230620100","volume":"100","author":"M Engel","year":"2003","unstructured":"Engel M, Hoffmann T, Wagner L, Wermann M, Heiser U, Kiefersauer R, et al. 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