Baseline β-catenin, programmed death-ligand 1 expression and tumour-infiltrating lymphocytes predict response and poor prognosis in BRAF inhibitor-treated melanoma patients

Eur J Cancer. 2017 Jun:78:70-81. doi: 10.1016/j.ejca.2017.03.012. Epub 2017 Apr 14.

Abstract

Background: The activation of oncogenic Wnt/β-catenin pathway in melanoma contributes to a lack of T-cell infiltration. Whether baseline β-catenin expression in the context of tumour-infiltrating lymphocytes (TILs) and programmed death ligand-1 (PD-L1) overexpression correlates with prognosis of metastatic melanoma patients (MMPs) treated with mitogen-activated protein kinase, MAPK inhibitor (MAPKi) monotherapy, however, has not been fully clarified.

Patients and methods: Sixty-four pre-treatment formalin-fixed and paraffin embedded melanoma samples from MMP treated with a BRAF inhibitor (n = 39) or BRAF and MEK inhibitors (n = 25) were assessed for presence of β-catenin, PD-L1, cluster of differentiation (CD)8, CD103 and forkhead box protein P3 (FOXP3) expression by immunohistochemistry, and results were correlated with clinical outcome. Quantitative assessment of mRNA transcripts associated with Wnt/β-catenin pathway and immune response was performed in 51 patients.

Results: We found an inverse correlation between tumoural β-catenin expression and the level of CD8, CD103 or forkhead box protein P3 (FOXP3) positivity in the tumour microenvironment (TME). By multivariate analysis, PD-L1 <5% (odds ratio, OR 0.12, 95% confidence interval, CI 0.03-0.53, p = 0.005) and the presence of CD8+ T cells (OR 18.27, 95%CI 2.54-131.52, p = 0.004) were significantly associated with a higher probability of response to MAPKi monotherapy. Responding patients showed a significantly increased expression of mRNA transcripts associated with adaptive immunity and antigen presentation. By multivariate analysis, progression-free survival (PFS) (hazards ratio (HR) = 0.25 95%CI 0.10-0.61, p = 0.002) and overall survival (OS) (HR = 0.24 95%CI 0.09-0.67, p = 0.006) were longer in patients with high density of CD8+ T cells and β-catenin <10% than those without CD8+ T cells infiltration and β-catenin ≥10%.

Conclusion: Our findings provide evidence that in the context of MAPKi monotherapy, immune subsets in the (TME) and gene signature predict prognosis in MMPs.

Keywords: BRAF inhibitors; Melanoma; T lymphocytes; prognosis; β-catenin.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Antigens, CD / metabolism
  • CD8 Antigens / metabolism
  • Female
  • Forkhead Transcription Factors / metabolism
  • Humans
  • Imidazoles / therapeutic use
  • Indoles / therapeutic use
  • Integrin alpha Chains / metabolism
  • Lymphocytes, Tumor-Infiltrating / physiology*
  • Male
  • Melanoma / drug therapy*
  • Melanoma / metabolism
  • Melanoma / mortality
  • Middle Aged
  • Mitogen-Activated Protein Kinase Kinases / antagonists & inhibitors
  • Oximes / therapeutic use
  • Prognosis
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor / metabolism*
  • Prospective Studies
  • Proto-Oncogene Proteins B-raf / antagonists & inhibitors
  • Pyridones / therapeutic use
  • Pyrimidinones / therapeutic use
  • Skin Neoplasms / drug therapy*
  • Skin Neoplasms / metabolism
  • Skin Neoplasms / mortality
  • Sulfonamides / therapeutic use
  • Treatment Outcome
  • Vemurafenib
  • Young Adult
  • beta Catenin / metabolism*

Substances

  • Antigens, CD
  • CD8 Antigens
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • Imidazoles
  • Indoles
  • Integrin alpha Chains
  • Oximes
  • Programmed Cell Death 1 Receptor
  • Pyridones
  • Pyrimidinones
  • Sulfonamides
  • alpha E integrins
  • beta Catenin
  • Vemurafenib
  • trametinib
  • BRAF protein, human
  • Proto-Oncogene Proteins B-raf
  • Mitogen-Activated Protein Kinase Kinases
  • dabrafenib