A novel ΔNp63-dependent immune mechanism improves prognosis of HPV-related head and neck cancer

Front Immunol. 2023 Oct 25:14:1264093. doi: 10.3389/fimmu.2023.1264093. eCollection 2023.

Abstract

Background: Deconvoluting the heterogenous prognosis of Human Papillomavirus (HPV)-related oropharyngeal squamous cell carcinoma (OSCC) is crucial for enhancing patient care, given its rapidly increasing incidence in western countries and the adverse side effects of OSCC treatments.

Methods: Transcriptomic data from HPV-positive OSCC samples were analyzed using unsupervised hierarchical clustering, and clinical relevance was evaluated using Kaplan-Meier analysis. HPV-positive OSCC cell line models were used in functional analyses and phenotypic assays to assess cell migration and invasion, response to cisplatin, and phagocytosis by macrophages in vitro.

Results: We found, by transcriptomic analysis of HPV-positive OSCC samples, a ΔNp63 dependent molecular signature that is associated with patient prognosis. ΔNp63 was found to act as a tumor suppressor in HPV-positive OSCC at multiple levels. It inhibits cell migration and invasion, and favors response to chemotherapy. RNA-Seq analysis uncovered an unexpected regulation of genes, such as DKK3, which are involved in immune response-signalling pathways. In agreement with these observations, we found that ΔNp63 expression levels correlate with an enhanced anti-tumor immune environment in OSCC, and ΔNp63 promotes cancer cell phagocytosis by macrophages through a DKK3/NF-κB-dependent pathway.

Conclusion: Our findings are the first comprehensive identification of molecular mechanisms involved in the heterogeneous prognosis of HPV-positive OSCC, paving the way for much-needed biomarkers and targeted treatment.

Keywords: human papillomavirus; immune response; oropharyngeal squamous cell carcinoma; tumor microenvironment; ΔNp63.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carcinoma, Squamous Cell*
  • Head and Neck Neoplasms* / genetics
  • Human Papillomavirus Viruses
  • Humans
  • Papillomavirus Infections* / complications
  • Prognosis
  • Squamous Cell Carcinoma of Head and Neck / genetics

Associated data

  • GEO/GSE190046

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was financially supported by the Centre National pour la Recherche Scientifique (CNRS, France; CG), Alsace Contre le Cancer, the Cancéropole Est and the Conférence de Coordination Interrégionale Grand Est-Bourgogne Franche-Comté de la Ligue Contre le Cancer. The Streinth Team is also supported by the Association pour la Recherche sur le Cancer, European action COST Proteocure, the Interdisciplinary thematic Institute InnoVec, the IDEX Excellence grant from Unistra, Itmo Cancer, and the Institut National du Cancer. JM is financially supported by a PhD fellowship awarded by the French national “Ligue Contre le Cancer”.