The IFN-γ/PD-L1 axis between T cells and tumor microenvironment: hints for glioma anti-PD-1/PD-L1 therapy

J Neuroinflammation. 2018 Oct 17;15(1):290. doi: 10.1186/s12974-018-1330-2.

Abstract

Background: PD-L1 is an immune inhibitory receptor ligand that leads to T cell dysfunction and apoptosis by binding to its receptor PD-1, which works in braking inflammatory response and conspiring tumor immune evasion. However, in gliomas, the cause of PD-L1 expression in the tumor microenvironment is not yet clear. Besides, auxiliary biomarkers are urgently needed for screening possible responsive glioma patients for anti-PD-1/PD-L1 therapies.

Methods: The distribution of tumor-infiltrating T cells and PD-L1 expression was analyzed via immunofluorescence in orthotopic murine glioma model. The expression of PD-L1 in immune cell populations was detected by flow cytometry. Data excavated from TCGA LGG/GBM datasets and the Ivy Glioblastoma Atlas Project was used for in silico analysis of the correlation among genes and survival.

Results: The distribution of tumor-infiltrating T cells and PD-L1 expression, which parallels in murine orthotopic glioma model and human glioma microdissections, was interrelated. The IFN-γ level was positively correlated with PD-L1 expression in murine glioma. Further, IFN-γ induces PD-L1 expression on primary cultured microglia, bone marrow-derived macrophages, and GL261 glioma cells in vitro. Seven IFN-γ-induced genes, namely GBP5, ICAM1, CAMK2D, IRF1, SOCS3, CD44, and CCL2, were selected to calculate as substitute indicator for IFN-γ level. By combining the relative expression of the listed IFN-γ-induced genes, IFN-γ score was positively correlated with PD-L1 expression in different anatomic structures of human glioma and in glioma of different malignancies.

Conclusion: Our study identified the distribution of tumor-infiltrating T cells and PD-L1 expression in murine glioma model and human glioma samples. And we found that IFN-γ is an important cause of PD-L1 expression in the glioma microenvironment. Further, we proposed IFN-γ score aggregated from the expressions of the listed IFN-γ-induced genes as a complementary prognostic indicator for anti-PD-1/PD-L1 therapy.

Keywords: Glioma; IFN-γ; Immune checkpoint; Immune evasion; PD-L1.

MeSH terms

  • Animals
  • B7-H1 Antigen / genetics
  • B7-H1 Antigen / metabolism*
  • Brain Neoplasms* / metabolism
  • Brain Neoplasms* / pathology
  • Brain Neoplasms* / therapy
  • CD8-Positive T-Lymphocytes / pathology*
  • Calcium-Binding Proteins / metabolism
  • Cells, Cultured
  • Coculture Techniques
  • Cytokines / genetics
  • Cytokines / metabolism
  • Disease Models, Animal
  • Gene Expression Regulation, Neoplastic / drug effects
  • Glioma* / metabolism
  • Glioma* / pathology
  • Glioma* / therapy
  • Interferon-gamma / metabolism*
  • Interferon-gamma / pharmacology
  • Macrophages / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Microfilament Proteins / metabolism
  • Microglia / physiology
  • Programmed Cell Death 1 Receptor / genetics
  • Programmed Cell Death 1 Receptor / metabolism*
  • RNA, Messenger / metabolism
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / physiology*

Substances

  • Aif1 protein, mouse
  • B7-H1 Antigen
  • Calcium-Binding Proteins
  • Cd274 protein, mouse
  • Cytokines
  • Microfilament Proteins
  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • RNA, Messenger
  • Interferon-gamma