VLA-4 suppression by senescence signals regulates meningeal immunity and leptomeningeal metastasis

Elife. 2022 Dec 9:11:e83272. doi: 10.7554/eLife.83272.

Abstract

Leptomeningeal metastasis is associated with dismal prognosis and has few treatment options. However, very little is known about the immune response to leptomeningeal metastasis. Here, by establishing an immunocompetent mouse model of breast cancer leptomeningeal metastasis, we found that tumor-specific CD8+ T cells were generated in deep cervical lymph nodes (dCLNs) and played an important role in controlling leptomeningeal metastasis. Mechanistically, T cells in dCLNs displayed a senescence phenotype and their recruitment was impaired in mice bearing cancer cells that preferentially colonized in leptomeningeal space. Upregulation of p53 suppressed the transcription of VLA-4 in senescent dCLN T cells and consequently inhibited their migration to the leptomeningeal compartment. Clinically, CD8+ T cells from the cerebrospinal fluid of patients with leptomeningeal metastasis exhibited senescence and VLA-4 downregulation. Collectively, our findings demonstrated that CD8+ T cell immunosenescence drives leptomeningeal metastasis.

Keywords: VLA-4; cancer biology; deep cervical lymph nodes; human; immunology; immunosenescence; inflammation; leptomeningeal metastasis; meningeal immunity; mouse.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes
  • Integrin alpha4beta1
  • Meningeal Neoplasms* / secondary
  • Meningeal Neoplasms* / therapy
  • Mice

Substances

  • Integrin alpha4beta1

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.