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Senescent cancer-associated fibroblasts in pancreatic adenocarcinoma restrict CD8+ T cell activation and limit responsiveness to immunotherapy in mice

Benjamin Assouline, Rachel E. Kahn, Lutfi Hodali, Reba Condiotti, Yarden Engel, Ela Elyada, Tzlil Mordechai-Heyn, Jason R. Pitarresi, Dikla Atias, Eliana Steinberg, Tirza Bidany-Mizrahi, Esther Forkosh, Lior H. Katz, Ofra Benny, Talia Golan, Matan Hofree, Sheila A. Stewart, Karine Atlan, Gideon Zamir, Ben Z. Stanger, Michael Berger, Ittai Ben‐Porath

2024Nature Communications78 citationsDOIOpen Access PDF

Abstract

Abstract Senescent cells within tumors and their stroma exert complex pro- and anti-tumorigenic functions. However, the identities and traits of these cells, and the potential for improving cancer therapy through their targeting, remain poorly characterized. Here, we identify a senescent subset within previously-defined cancer-associated fibroblasts (CAFs) in pancreatic ductal adenocarcinomas (PDAC) and in premalignant lesions in mice and humans. Senescent CAFs isolated from mouse and humans expressed elevated levels of immune-regulatory genes. Depletion of senescent CAFs, either genetically or using the Bcl-2 inhibitor ABT-199 (venetoclax), increased the proportion of activated CD8 + T cells in mouse pancreatic carcinomas, whereas induction of CAF senescence had the opposite effect. Combining ABT-199 with an immune checkpoint therapy regimen significantly reduced mouse tumor burden. These results indicate that senescent CAFs in PDAC stroma limit the numbers of activated cytotoxic CD8 + T cells, and suggest that their targeted elimination through senolytic treatment may enhance immunotherapy.

Topics & Concepts

Cancer researchCytotoxic T cellImmunotherapyPancreatic cancerCD8StromaImmune systemBiologyCancerCancer-Associated FibroblastsCancer immunotherapyAdenocarcinomaTumor microenvironmentImmunologyImmunohistochemistryGeneticsBiochemistryIn vitroImmune cells in cancerImmunotherapy and Immune ResponsesEpigenetics and DNA Methylation
Senescent cancer-associated fibroblasts in pancreatic adenocarcinoma restrict CD8+ T cell activation and limit responsiveness to immunotherapy in mice | Litcius