Cited by 151Cancer Immunotherapy and BiomarkersT-cell and B-cell ImmunologyImmunotherapy and Immune Responses

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Neuropilin-1 is a T cell memory checkpoint limiting long-term antitumor immunity

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Liu, Chang, Somasundaram, Ashwin, Manne, Sasikanth, Gocher, Angela M., Szymczak-Workman, Andrea L., Vignali, Kate M., Scott, Ellen N., Normolle, Daniel P., John Wherry, E., Lipson, Evan J., Ferris, Robert L., Bruno, Tullia C., Workman, Creg J., Vignali, Dario A. A.·2020·Nature Immunology

DOI 10.1038/s41590-020-0733-2PMC PMC7442600

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Abstract

Robust CD8+ T cell memory is essential for long-term protective immunity but is often compromised in cancer, where T cell exhaustion leads to loss of memory precursors. Immunotherapy via checkpoint blockade may not effectively reverse this defect, potentially underlying disease relapse. Here we report that mice with a CD8+ T cell-restricted neuropilin-1 (NRP1) deletion exhibited substantially enhanced protection from tumor rechallenge and sensitivity to anti-PD1 immunotherapy, despite unchanged primary tumor growth. Mechanistically, NRP1 cell-intrinsically limited the self-renewal of the CD44+PD1+TCF1+TIM3- progenitor exhausted T cells, which was associated with their reduced ability to induce c-Jun/AP-1 expression on T cell receptor restimulation, a mechanism that may contribute to terminal T cell exhaustion at the cost of memory differentiation in wild-type tumor-bearing hosts. These data indicate that blockade of NRP1, a unique 'immune memory checkpoint', may promote the development of long-lived tumor-specific T mem that are essential for durable antitumor immunity.

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Authors: Liu, C., Somasundaram, A., Manne, S., Gocher, A. M., Szymczak-Workman, A. L., Vignali, K. M., Scott, E. N., Normolle, D. P., John Wherry, E., Lipson, E. J., Ferris, R. L., Bruno, T. C., Workman, C. J., & Vignali, D. A. A.
Affiliations: University of Pittsburgh (US)
University of Pennsylvania (US)
UPMC Hillman Cancer Center (US)
Johns Hopkins University (US)
Corresponding author: Vignali, Dario A. A.
ORCID: Liu, Chang
Somasundaram, Ashwin
Manne, Sasikanth
Szymczak-Workman, Andrea L.
Vignali, Kate M.
Scott, Ellen N.
Normolle, Daniel P.
John Wherry, E.
Lipson, Evan J.
Ferris, Robert L.
Bruno, Tullia C.
Workman, Creg J.
Vignali, Dario A. A.
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2020-07-13
Volume: 21
Issue: 9
Pages: 1010-1021
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/s41590-020-0733-2
PMC: PMC7442600
OpenAlex: W3040823189
Cited by: 151
References: 56
Citations by year: 2026: 13 · 2025: 36 · 2024: 18 · 2023: 27 · 2022: 31 · 2021: 20 · 2020: 6
FWCI: 7.59
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Immunology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: U.S. Department of Health & Human Services | National Institutes of Health (CA203689, AI108545, CA082084, CA247004-01, AI117950, AI082630, AI112521, AI115712, CA210944)
U.S. Department of Health & Human Services | NIH | National Cancer Institute (CA047904, CA006973, CA097190)
Topics: Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords: neuropilin-1, T cell exhaustion, CD8+ T cell memory, immune checkpoint, antitumor immunity, anti-PD-1 therapy, tumor rechallenge, T cell self-renewal
MeSH terms: Immune Checkpoint Proteins, Animals, Humans, Immune Tolerance, Immunity, Immunologic Memory, Melanoma, Experimental, Signal Transduction, Mice, Knockout, CD8-Positive T-Lymphocytes, Neuropilin-1, Cell Line, Tumor, Mice, Precursor Cells, T-Lymphoid, Programmed Cell Death 1 Receptor

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Neuropilin-1 is a T cell memory checkpoint limiting long-term antitumor immunity

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