In-depth characterization of the tumor microenvironment in central nervous system lymphoma reveals implications for immune-checkpoint therapy

Cancer Immunol Immunother. 2020 Sep;69(9):1751-1766. doi: 10.1007/s00262-020-02575-y. Epub 2020 Apr 25.

Abstract

Primary central nervous system lymphoma (PCNSL) is a rare type of non-Hodgkin lymphoma with an aggressive clinical course. To investigate the potential of immune-checkpoint therapy, we retrospectively studied the tumor microenvironment (TME) using high-plex immunohistochemistry in 22 PCNSL and compared to 7 secondary CNS lymphomas (SCNSL) and 7 "other" CNSL lymphomas with the presence of the Epstein-Barr virus and/or compromised immunity. The TME in PCNSL was predominantly composed of CD8+ cytotoxic T cells and CD163+ phagocytes. Despite molecular differences between PCNSL and SCNSL, the cellular composition and the functional spectrum of cytotoxic T cells were similar. But cytotoxic T cell activation was significantly influenced by pre-biopsy corticosteroids intake, tumor expression of PD-L1 and the presence of EBV. The presence of low numbers of CD8+ T cells and geographic-type necrosis each predicted inferior outcome in PCNSL. Both M1-like (CD68 + CD163low) and M2-like (CD68 + CD163high) phagocytes were identified, and an increased ratio of M1-like/M2-like phagocytes was associated with a better survival. PD-L1 was expressed in lymphoma cells in 28% of cases, while PD1 was expressed in only 0.4% of all CD8+ T cells. TIM-3, a marker for T cell exhaustion, was significantly more expressed in CD8posPD-1pos T cells compared to CD8posPD-1neg T cells, and a similar increased expression was observed in M2-like pro-tumoral phagocytes. In conclusion, the clinical impact of TME composition supports the use of immune-checkpoint therapies in PCNSL. Based on observed differences in immune-checkpoint expression, combinations that boost cytotoxic T cell activation (by blocking TIM-3 or TGFBR1) prior to the administration of PD-L1 inhibition could be of interest.

Keywords: Immunotherapy; PCNSL; Primary central nervous system lymphoma; TILS; TME; Tumor microenvironment.

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Aged, 80 and over
  • Antigens, CD / immunology
  • Antigens, Differentiation, Myelomonocytic / immunology
  • Biomarkers, Tumor / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • Central Nervous System Neoplasms / immunology*
  • Central Nervous System Neoplasms / therapy*
  • Central Nervous System Neoplasms / virology
  • Child
  • Female
  • Herpesvirus 4, Human / pathogenicity
  • Humans
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Lymphoma / immunology*
  • Lymphoma / therapy*
  • Lymphoma / virology
  • Male
  • Middle Aged
  • Receptors, Cell Surface / immunology
  • Retrospective Studies
  • T-Lymphocytes, Cytotoxic / immunology
  • Tumor Microenvironment / immunology*
  • Young Adult

Substances

  • Antigens, CD
  • Antigens, Differentiation, Myelomonocytic
  • Biomarkers, Tumor
  • CD163 antigen
  • Receptors, Cell Surface