Immune response and evasion mechanisms in lip carcinogenesis: An immunohistochemical study

Arch Oral Biol. 2019 Feb:98:99-107. doi: 10.1016/j.archoralbio.2018.09.017. Epub 2018 Sep 29.

Abstract

Objectives: Programmed death ligand-1 (PD-L1) and human leukocyte antigen-G (HLA-G) are considered immune checkpoint molecules that inhibit T-cell effectiveness, contributing to tumor immune escape. This study investigated PD-L1, HLA-G, CD8, and granzyme B (GrB) expression at different stages of lip carcinogenesis.

Design and results: Forty cases of lip squamous cell carcinoma (LSCC), 55 actinic cheilitis (AC), and 10 healthy lip mucosa (HLM) were submitted to immunohistochemistry. Semiquantitative (PD-L1, HLA-G), and quantitative (CD8, GrB) analysis were performed. PD-L1 and HLA-G expression in neoplastic cells/keratinocytes and stroma/connective tissue was significantly higher in LSCC and AC, compared to HLM (p<0.05). PD-L1 was not associated with clinicopathological features of the lesions. HLA-G expression by malignant cells was significantly higher in LSCCs with distant metastasis (p = 0.041).CD8+ and GrB+ cell numbers progressively increased from HLMs to LSCC, with AC exhibiting intermediate numbers (p<0.01). Most LSCCs showed coexistence of PD-L1+ and CD8+ cells (72.5%). PD-L1 was directly correlated to CD8+ and GrB+ lymphocytic infiltration in LSCCs (p<0.05). Low cytotoxic immune response was associated with lymph node metastasis in LSCC (p<0.05).

Conclusions: PD-L1 and HLA-G-mediated immune evasion mechanisms are likely to occur from early pre-malignant to advanced malignant stages of lip carcinogenesis, which might provide a rationale for therapeutic blockade of these pathways. PD-L1 expression in LSCCs was correlated with the cytotoxic markers, suggesting that PD-L1 may appear as an escape mechanism in response to an active antitumor response.

Keywords: Cheilitis, lip carcinogenesis; HLA-G; PD-L1; Squamous cell carcinoma; Tumor-infiltrating lymphocytes.

MeSH terms

  • CD8-Positive T-Lymphocytes / immunology
  • Carcinogenesis / immunology*
  • Carcinoma, Squamous Cell / immunology
  • Carcinoma, Squamous Cell / pathology
  • Cheilitis / immunology
  • Cheilitis / pathology
  • Cross-Sectional Studies
  • Female
  • Granzymes / immunology
  • HLA-G Antigens / immunology
  • Humans
  • Immune Evasion
  • Immunohistochemistry
  • Keratinocytes / immunology
  • Keratinocytes / pathology
  • Lip Neoplasms / immunology*
  • Lip Neoplasms / pathology
  • Lymphatic Metastasis
  • Male
  • Middle Aged
  • Mouth Mucosa / immunology
  • Mouth Mucosa / pathology
  • Programmed Cell Death 1 Receptor / immunology
  • Retrospective Studies
  • Stromal Cells / immunology
  • Stromal Cells / pathology
  • Tumor Microenvironment / immunology

Substances

  • HLA-G Antigens
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor
  • Granzymes

Supplementary concepts

  • Actinic cheilitis