Spatial cellular order underlies locally-confined mechanisms of immune resistance in oropharyngeal cancer

Nat Commun. 2026 Jun 13;17(1):7512. doi: 10.1038/s41467-026-74318-z.

Abstract

Oropharyngeal squamous cell carcinomas (OPSCCs) frequently result from oncogenic human papilloma virus (HPV) infections (HPV-OPSCC). The mechanisms underlying effective immune escape, despite abundant viral antigens, are incompletely understood. Here, we performed single-cell spatial gene expression profiling of HPV-OPSCC to characterize cellular organization and mechanisms of immune resistance. We describe distinct tumor-parenchymal immune foci that differ in cytokine expression, spatial location, immune cell infiltration and cancer cell states. Furthermore, immune foci display profound differences related to co-inhibitory receptor signaling and immunosuppressive myeloid cells, suggesting that different tumor-parenchymal regions may be dominated by distinct, locally-confined mechanisms of immunosuppression. Additionally, senescent-like HPV-OPSCC cells lacking HPV transcripts (HPVoff) are evident across the tumor parenchyma and able to evade HPV-specific T cell-mediated immunity in vitro. HPVoff cells are enriched within hypoxic regions and near IFN-γ producing T cells suggesting that both hypoxia and IFN-γ signaling can promote the HPVoff phenotype. In conclusion, our findings highlight a complex cellular interplay underlying heterogeneous cancer cell states, spatial immune cell organization, and diverse mechanisms of immune escape.

MeSH terms

  • Carcinoma, Squamous Cell* / genetics
  • Carcinoma, Squamous Cell* / immunology
  • Carcinoma, Squamous Cell* / pathology
  • Carcinoma, Squamous Cell* / virology
  • Cell Line, Tumor
  • Cytokines / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic
  • Human Papillomavirus Viruses / genetics
  • Human Papillomavirus Viruses / immunology
  • Humans
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism
  • Oropharyngeal Neoplasms* / genetics
  • Oropharyngeal Neoplasms* / immunology
  • Oropharyngeal Neoplasms* / pathology
  • Oropharyngeal Neoplasms* / virology
  • Papillomavirus Infections* / immunology
  • Papillomavirus Infections* / virology
  • Signal Transduction
  • Single-Cell Analysis
  • T-Lymphocytes / immunology
  • Tumor Escape* / genetics
  • Tumor Escape* / immunology
  • Tumor Microenvironment / genetics
  • Tumor Microenvironment / immunology

Substances

  • Interferon-gamma
  • Cytokines