Multipanel mass cytometry reveals anti-PD-1 therapy-mediated B and T cell compartment remodeling in tumor-draining lymph nodes

JCI Insight. 2020 Jan 30;5(2):e132286. doi: 10.1172/jci.insight.132286.

Abstract

Anti-programmed cell death protein 1 (anti-PD-1) therapy has become an immunotherapeutic backbone for treating many cancer types. Although many studies have aimed to characterize the immune response to anti-PD-1 therapy in the tumor and in the peripheral blood, relatively less is known about the changes in the tumor-draining lymph nodes (TDLNs). TDLNs are primary sites of tumor antigen exposure that are critical to both regulation and cross-priming of the antitumor immune response. We used multipanel mass cytometry to obtain a high-parameter proteomic (39 total unique markers) immune profile of the TDLNs in a well-studied PD-1-responsive, immunocompetent mouse model. Based on combined hierarchal gating and unsupervised clustering analyses, we found that anti-PD-1 therapy enhances remodeling of both B and T cell compartments toward memory phenotypes. Functionally, expression of checkpoint markers was increased in conjunction with production of IFN-γ, TNF-α, or IL-2 in key cell types, including B and T cell subtypes, and rarer subsets, such as Tregs and NKT cells. A deeper profiling of the immunologic changes that occur in the TDLN milieu during effective anti-PD-1 therapy may lead to the discovery of novel biomarkers for monitoring response and provide key insights toward developing combination immunotherapeutic strategies.

Keywords: B cells; Immunology; Lymph; Oncology; T cells.

MeSH terms

  • Animals
  • Antibodies, Neoplasm / immunology*
  • Antibodies, Neoplasm / pharmacology*
  • Antibodies, Neoplasm / therapeutic use
  • B-Lymphocytes / immunology*
  • Female
  • Interferon-gamma / metabolism
  • Interleukin-2 / metabolism
  • Lymph Nodes / drug effects*
  • Lymph Nodes / immunology
  • Lymph Nodes / pathology
  • Mice
  • Mice, Inbred C57BL
  • Natural Killer T-Cells
  • Neoplasms / drug therapy
  • Neoplasms / immunology*
  • Programmed Cell Death 1 Receptor / drug effects*
  • Proteomics
  • T-Lymphocytes / immunology*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Antibodies, Neoplasm
  • Interleukin-2
  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma