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The remission status of AML patients after allo-HCT is associated with a distinct single-cell bone marrow T-cell signature

Acute myeloid leukemia (AML) is a hematologic malignancy for which allogeneic hematopoietic cell transplantation (allo-HCT) often remains the only curative therapeutic approach. However, incapability of T cells to recognize and eliminate residual leukemia stem cells might lead to an insufficient gra...

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Main Authors: Mathioudaki, Anna (Author) , Wang, Xizhe (Author) , Sedloev, David (Author) , Huth, Richard (Author) , Kamal, Aryan (Author) , Hundemer, Michael (Author) , Liu, Yi (Author) , Vasileiou, Spyridoula (Author) , Lulla, Premal (Author) , Müller-Tidow, Carsten (Author) , Dreger, Peter (Author) , Luft, Thomas (Author) , Sauer, Tim (Author) , Schmitt, Michael (Author) , Zaugg, Judith B. (Author) , Pabst, Caroline (Author)
Format: Article (Journal)
Language:English
Published: March 28 2024
In: Blood
Year: 2024, Volume: 143, Issue: 13, Pages: 1269-1281
ISSN:1528-0020
DOI:10.1182/blood.2023021815
Online Access:Verlag, lizenzpflichtig, Volltext: https://doi.org/10.1182/blood.2023021815
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Author Notes:Anna Mathioudaki, Xizhe Wang, David Sedloev, Richard Huth, Aryan Kamal, Michael Hundemer, Yi Liu, Spyridoula Vasileiou, Premal Lulla, Carsten Müller-Tidow, Peter Dreger, Thomas Luft, Tim Sauer, Michael Schmitt, Judith B. Zaugg, and Caroline Pabst

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520 |a Acute myeloid leukemia (AML) is a hematologic malignancy for which allogeneic hematopoietic cell transplantation (allo-HCT) often remains the only curative therapeutic approach. However, incapability of T cells to recognize and eliminate residual leukemia stem cells might lead to an insufficient graft-versus-leukemia (GVL) effect and relapse. Here, we performed single-cell RNA-sequencing (scRNA-seq) on bone marrow (BM) T lymphocytes and CD34+ cells of 6 patients with AML 100 days after allo-HCT to identify T-cell signatures associated with either imminent relapse (REL) or durable complete remission (CR). We observed a higher frequency of cytotoxic CD8+ effector and gamma delta (γδ) T cells in CR vs REL samples. Pseudotime and gene regulatory network analyses revealed that CR CD8+ T cells were more advanced in maturation and had a stronger cytotoxicity signature, whereas REL samples were characterized by inflammatory tumor necrosis factor/NF-κB signaling and an immunosuppressive milieu. We identified ADGRG1/GPR56 as a surface marker enriched in CR CD8+ T cells and confirmed in a CD33-directed chimeric antigen receptor T cell/AML coculture model that GPR56 becomes upregulated on T cells upon antigen encounter and elimination of AML cells. We show that GPR56 continuously increases at the protein level on CD8+ T cells after allo-HCT and confirm faster interferon gamma (IFN-γ) secretion upon re-exposure to matched, but not unmatched, recipient AML cells in the GPR56+ vs GPR56- CD8+ T-cell fraction. Together, our data provide a single-cell reference map of BM-derived T cells after allo-HCT and propose GPR56 expression dynamics as a surrogate for antigen encounter after allo-HCT. 
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