SPHK1 promotes HNSCC immune evasion by regulating the MMP1-PD-L1 axis

Theranostics. 2024 Oct 28;14(18):7199-7218. doi: 10.7150/thno.102390. eCollection 2024.

Abstract

Rationale: Immune checkpoint inhibitors (ICIs) have demonstrated significant efficacy against head and neck squamous cell carcinoma (HNSCC), but their overall response rate (ORR) remains limited. Previous studies have highlighted the crucial role of sphingosine kinases (SPHKs) in the tumor microenvironment (TME); however, their function in immunotherapy remains unclear. Methods: We conducted comprehensive bioinformatics analysis, functional studies, and clinical validation, to investigate the role of SPHK1 in the immunology of HNSCC. Results: Functionally, SPHK1 significantly promoted tumor growth by inhibiting anti-tumor immunity in immune-competent HNSCC mouse models and tumor-T cell co-cultures. Mechanistic analysis revealed that SPHK1 regulated matrix metalloproteinase-1 (MMP1) expression via the MAPK1 pathway, which subsequently influenced tumor programmed cell death ligand 1 (PD-L1) expression. Furthermore, SPHK1 and MMP1 could predict the efficacy of programmed cell death 1 monoclonal antibody (PD-1 mAb) immunotherapy in HNSCC and were independent risk factors for survival in patients with HNSCC. Conclusion: Our study reveals a novel role for SPHK1 in mediating immune evasion in HNSCC through the regulation of the MMP1-PD-L1 axis. We identified SPHK1 and MMP1 as predictive biomarkers for the therapeutic response to PD-1 mAb and provided new therapeutic targets for patients with HNSCC.

Keywords: HNSCC; MMP1; PD-1.; PD-L1; SPHK1.

MeSH terms

  • Animals
  • B7-H1 Antigen* / metabolism
  • Cell Line, Tumor
  • Female
  • Head and Neck Neoplasms* / immunology
  • Head and Neck Neoplasms* / metabolism
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Immune Evasion
  • Immunotherapy / methods
  • Male
  • Matrix Metalloproteinase 1* / genetics
  • Matrix Metalloproteinase 1* / metabolism
  • Mice
  • Phosphotransferases (Alcohol Group Acceptor)* / metabolism
  • Squamous Cell Carcinoma of Head and Neck* / drug therapy
  • Squamous Cell Carcinoma of Head and Neck* / immunology
  • Squamous Cell Carcinoma of Head and Neck* / metabolism
  • Tumor Escape
  • Tumor Microenvironment* / immunology

Substances

  • B7-H1 Antigen
  • Matrix Metalloproteinase 1
  • Phosphotransferases (Alcohol Group Acceptor)
  • CD274 protein, human
  • sphingosine kinase
  • MMP1 protein, human
  • Immune Checkpoint Inhibitors
  • Sphk1 protein, mouse