Intratumor heterogeneity and T cell exhaustion in primary CNS lymphoma

Genome Med. 2022 Sep 24;14(1):109. doi: 10.1186/s13073-022-01110-1.

Abstract

Background: Primary central nervous system lymphoma (PCNSL) is a rare lymphoma of the central nervous system, usually of diffuse large B cell phenotype. Stereotactic biopsy followed by histopathology is the diagnostic standard. However, limited material is available from CNS biopsies, thus impeding an in-depth characterization of PCNSL.

Methods: We performed flow cytometry, single-cell RNA sequencing, and B cell receptor sequencing of PCNSL cells released from biopsy material, blood, and cerebrospinal fluid (CSF), and spatial transcriptomics of biopsy samples.

Results: PCNSL-released cells were predominantly activated CD19+CD20+CD38+CD27+ B cells. In single-cell RNA sequencing, PCNSL cells were transcriptionally heterogeneous, forming multiple malignant B cell clusters. Hyperexpanded B cell clones were shared between biopsy- and CSF- but not blood-derived cells. T cells in the tumor microenvironment upregulated immune checkpoint molecules, thereby recognizing immune evasion signals from PCNSL cells. Spatial transcriptomics revealed heterogeneous spatial organization of malignant B cell clusters, mirroring their transcriptional heterogeneity across patients, and pronounced expression of T cell exhaustion markers, co-localizing with a highly malignant B cell cluster.

Conclusions: Malignant B cells in PCNSL show transcriptional and spatial intratumor heterogeneity. T cell exhaustion is frequent in the PCNSL microenvironment, co-localizes with malignant cells, and highlights the potential of personalized treatments.

Keywords: Flow cytometry; Intratumoral heterogeneity; Primary central nervous system lymphoma; Single-cell RNA sequencing; Spatial transcriptomics; T cell exhaustion.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Central Nervous System Neoplasms* / diagnosis
  • Central Nervous System Neoplasms* / genetics
  • Central Nervous System Neoplasms* / pathology
  • Humans
  • Immune Checkpoint Proteins
  • Lymphoma* / diagnosis
  • Lymphoma* / genetics
  • Lymphoma* / pathology
  • Receptors, Antigen, B-Cell
  • T-Lymphocytes
  • Tumor Microenvironment

Substances

  • Immune Checkpoint Proteins
  • Receptors, Antigen, B-Cell