Senescence-associated lineage-aberrant plasticity evokes T-cell-mediated tumor control

Nat Commun. 2025 Mar 31;16(1):3079. doi: 10.1038/s41467-025-57429-x.

Abstract

Cellular senescence is a stress-inducible state switch relevant in aging, tumorigenesis and cancer therapy. Beyond a lasting arrest, senescent cells are characterized by profound chromatin remodeling and transcriptional reprogramming. We show here myeloid-skewed aberrant lineage plasticity and its immunological ramifications in therapy-induced senescence (TIS) of primary human and murine B-cell lymphoma. We find myeloid transcription factor (TF) networks, specifically AP-1-, C/EBPβ- and PU.1-governed transcriptional programs, enriched in TIS but not in equally chemotherapy-exposed senescence-incapable cancer cells. Dependent on these master TF, TIS lymphoma cells adopt a lineage-promiscuous state with properties of monocytic-dendritic cell (DC) differentiation. TIS lymphoma cells are preferentially lysed by T-cells in vitro, and mice harboring DC-skewed Eμ-myc lymphoma experience significantly longer tumor-free survival. Consistently, superior long-term outcome is also achieved in diffuse large B-cell lymphoma patients with high expression of a TIS-related DC signature. In essence, these data demonstrate a therapeutically exploitable, prognostically favorable immunogenic role of senescence-dependent aberrant myeloid plasticity in B-cell lymphoma.

MeSH terms

  • Animals
  • Cell Differentiation
  • Cell Line, Tumor
  • Cell Lineage
  • Cell Plasticity
  • Cellular Senescence* / genetics
  • Cellular Senescence* / immunology
  • Dendritic Cells / immunology
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Lymphoma, B-Cell* / genetics
  • Lymphoma, B-Cell* / immunology
  • Lymphoma, B-Cell* / pathology
  • Lymphoma, Large B-Cell, Diffuse / genetics
  • Lymphoma, Large B-Cell, Diffuse / immunology
  • Lymphoma, Large B-Cell, Diffuse / pathology
  • Mice
  • Mice, Inbred C57BL
  • Proto-Oncogene Proteins
  • T-Lymphocytes* / immunology
  • Trans-Activators

Substances

  • proto-oncogene protein Spi-1
  • Proto-Oncogene Proteins
  • Trans-Activators