Cited by 306T-cell and B-cell ImmunologyCancer Immunotherapy and BiomarkersImmunotherapy and Immune Responses

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Two subsets of stem-like CD8+ memory T cell progenitors with distinct fate commitments in humans

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Galletti, Giovanni, De Simone, Gabriele, Mazza, Emilia M. C., Puccio, Simone, Mezzanotte, Claudia, Bi, Timothy M., Davydov, Alexey N., Metsger, Maria, Scamardella, Eloise, Alvisi, Giorgia, De Paoli, Federica, Zanon, Veronica, Scarpa, Alice, Camisa, Barbara, Colombo, Federico S., Anselmo, Achille, Peano, Clelia, Polletti, Sara, Mavilio, Domenico, Gattinoni, Luca, Boi, Shannon K., Youngblood, Benjamin A., Jones, Rhiannon E., Baird, Duncan M., Gostick, Emma, Llewellyn-Lacey, Sian, Ladell, Kristin, Price, David A., Chudakov, Dmitriy M., Newell, Evan W., Casucci, Monica, Lugli, Enrico·2020·Nature Immunology

DOI 10.1038/s41590-020-0791-5PMC PMC7610790

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Abstract

T cell memory relies on the generation of antigen-specific progenitors with stem-like properties. However, the identity of these progenitors has remained unclear, precluding a full understanding of the differentiation trajectories that underpin the heterogeneity of antigen-experienced T cells. We used a systematic approach guided by single-cell RNA-sequencing data to map the organizational structure of the human CD8+ memory T cell pool under physiological conditions. We identified two previously unrecognized subsets of clonally, epigenetically, functionally, phenotypically and transcriptionally distinct stem-like CD8+ memory T cells. Progenitors lacking the inhibitory receptors programmed death-1 (PD-1) and T cell immunoreceptor with Ig and ITIM domains (TIGIT) were committed to a functional lineage, whereas progenitors expressing PD-1 and TIGIT were committed to a dysfunctional, exhausted-like lineage. Collectively, these data reveal the existence of parallel differentiation programs in the human CD8+ memory T cell pool, with potentially broad implications for the development of immunotherapies and vaccines.

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Tosello, J., Richer, W., Missolo-Koussou, Y., Bonnin, E., Lemoine, S., Pretti, M. A. M., Ramos, R. N., Denizeau, J., Baulande, S., Bohec, M., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.17.674622
Additional file 4 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633562
Additional file 6 of The effect of metformin on senescence of T lymphocytes
Yang, J., Liu, H.-C., Zhang, J.-Q., Zou, J.-Y., Zhang, X., Chen, W.-M., Gu, Y., & Hong, H. (2024) · Figshare · doi:10.6084/m9.figshare.26652471
Additional file 11 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633583
Additional file 7 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633571
Additional file 5 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633565
Additional file 3 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633559
Additional file 12 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633586
Additional file 15 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633595
Additional file 9 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633577
Additional file 2 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.24455007
Additional file 2 of GITR and TIGIT immunotherapy provokes divergent multicellular responses in the tumor microenvironment of gastrointestinal cancers
Sathe, A., Ayala, C. I., Bai, X., Grimes, S. M., Lee, B., Kin, C., Shelton, A. A., Poultsides, G. A., & Ji, H. P. (2024) · Figshare · doi:10.6084/m9.figshare.24636707
Additional file 8 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633574
Additional file 2 of The effect of metformin on senescence of T lymphocytes
Yang, J., Liu, H.-C., Zhang, J.-Q., Zou, J.-Y., Zhang, X., Chen, W.-M., Gu, Y., & Hong, H. (2024) · Figshare · doi:10.6084/m9.figshare.24798069
Additional file 3 of The effect of metformin on senescence of T lymphocytes
Yang, J., Liu, H.-C., Zhang, J.-Q., Zou, J.-Y., Zhang, X., Chen, W.-M., Gu, Y., & Hong, H. (2024) · Figshare · doi:10.6084/m9.figshare.26652462
Additional file 10 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633580
Additional file 1 of The effect of metformin on senescence of T lymphocytes
Yang, J., Liu, H.-C., Zhang, J.-Q., Zou, J.-Y., Zhang, X., Chen, W.-M., Gu, Y., & Hong, H. (2023) · Figshare · doi:10.6084/m9.figshare.24797813
Additional file 5 of The effect of metformin on senescence of T lymphocytes
Yang, J., Liu, H.-C., Zhang, J.-Q., Zou, J.-Y., Zhang, X., Chen, W.-M., Gu, Y., & Hong, H. (2024) · Figshare · doi:10.6084/m9.figshare.26652468
Additional file 14 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633592
Additional file 4 of The effect of metformin on senescence of T lymphocytes
Yang, J., Liu, H.-C., Zhang, J.-Q., Zou, J.-Y., Zhang, X., Chen, W.-M., Gu, Y., & Hong, H. (2024) · Figshare · doi:10.6084/m9.figshare.26652465
Additional file 13 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633589
Additional file 6 of CD28/PD1 co-expression: dual impact on CD8+ T cells in peripheral blood and tumor tissue, and its significance in NSCLC patients' survival and ICB response
Palermo, B., Franzese, O., Frisullo, G., D’Ambrosio, L., Panetta, M., Campo, G., D’Andrea, D., Sperduti, I., De Nicola, F., Goeman, F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26633568
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Authors: Galletti, G., De Simone, G., Mazza, E. M. C., Puccio, S., Mezzanotte, C., Bi, T. M., Davydov, A. N., Metsger, M., Scamardella, E., Alvisi, G., De Paoli, F., Zanon, V., Scarpa, A., Camisa, B., Colombo, F. S., Anselmo, A., Peano, C., Polletti, S., Mavilio, D., Gattinoni, L., Boi, S. K., Youngblood, B. A., Jones, R. E., Baird, D. M., Gostick, E., Llewellyn-Lacey, S., Ladell, K., Price, D. A., Chudakov, D. M., Newell, E. W., Casucci, M., & Lugli, E.
Affiliations: IRCCS Humanitas Research Hospital (IT)
IRCCS Ospedale San Raffaele (IT)
Fred Hutch Cancer Center (US)
Central European Institute of Technology (CZ)
National Research Council (IT)
Humanitas University (IT)
University of Milan (IT)
National Institutes of Health (US)
St. Jude Children's Research Hospital (US)
Cardiff University (GB)
Skolkovo Institute of Science and Technology (RU)
Corresponding author: Lugli, Enrico
ORCID: Galletti, Giovanni
Mazza, Emilia M. C.
Puccio, Simone
Bi, Timothy M.
Davydov, Alexey N.
Metsger, Maria
Alvisi, Giorgia
Zanon, Veronica
Scarpa, Alice
Camisa, Barbara
Colombo, Federico S.
Anselmo, Achille
Peano, Clelia
Polletti, Sara
Mavilio, Domenico
Gattinoni, Luca
Boi, Shannon K.
Youngblood, Benjamin A.
Baird, Duncan M.
Ladell, Kristin
Price, David A.
Chudakov, Dmitriy M.
Newell, Evan W.
Casucci, Monica
Lugli, Enrico
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2020-10-12
Volume: 21
Issue: 12
Pages: 1552-1562
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/s41590-020-0791-5
PMC: PMC7610790
OpenAlex: W3092341078
Cited by: 299
References: 74
Citations by year: 2026: 31 · 2025: 49 · 2024: 66 · 2023: 53 · 2022: 51 · 2021: 46 · 2020: 3
FWCI: 13.55
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Immunology (publishedVersion)
PubMed (publishedVersion)
ORCA Online Research @Cardiff (Cardiff University) (acceptedVersion)
PubMed Central (acceptedVersion)
Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
University of Regensburg Publication Server (University of Regensburg) (submittedVersion)
ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
Zenodo (CERN European Organization for Nuclear Research) (submittedVersion)
Funders: Wellcome Trust (100326, 100326/Z/12/Z)
Cancer Research UK (C17199/A18246/A29202, 29202, 18246)
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords: memory CD8+ T cells, T cell exhaustion, PD-1, TIGIT, T cell differentiation, inhibitory receptors, single-cell RNA sequencing
MeSH terms: Animals, Cell Differentiation, Humans, Immunologic Memory, Biomarkers, Immunophenotyping, T-Lymphocyte Subsets, CD8-Positive T-Lymphocytes, Computational Biology, Gene Expression Profiling, Mice, Lymphoid Progenitor Cells, High-Throughput Nucleotide Sequencing, Telomere Homeostasis

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Two subsets of stem-like CD8+ memory T cell progenitors with distinct fate commitments in humans

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