Tissue-Resident Memory T Cells Mediate Immune Homeostasis in the Human Pancreas through the PD-1/PD-L1 Pathway

Cell Rep. 2019 Dec 17;29(12):3916-3932.e5. doi: 10.1016/j.celrep.2019.11.056.

Abstract

Non-recirculating tissue-resident memory T cells (TRMs) are the predominant T cell subset in diverse tissue sites, where they mediate protective immune responses in situ. Here, we reveal a role for TRM in maintaining immune homeostasis in the human pancreas through interactions with resident macrophages and the PD-1/PD-L1 inhibitory pathway. Using tissues obtained from organ donors, we identify that pancreas T cells comprise CD8+PD-1hi TRMs, which are phenotypically, functionally, and transcriptionally distinct compared to TRMs in neighboring jejunum and lymph node sites. Pancreas TRMs cluster with resident macrophages throughout the exocrine areas; TRM effector functions are enhanced by macrophage-derived co-stimulation and attenuated by the PD-1/PD-L1 pathways. Conversely, in samples from chronic pancreatitis, TRMs exhibit reduced PD-1 expression and reduced interactions with macrophages. These findings suggest important roles for PD-1 and TRM-macrophage interactions in controlling tissue homeostasis and immune dysfunctions underlying inflammatory disease, with important implications for PD-1-based immunotherapies.

Keywords: PD-1; chronic pancreatitis; macrophage; memory T cells; mucosal immunity; pancreas; tissue immunity.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • B7-H1 Antigen / genetics
  • B7-H1 Antigen / metabolism*
  • CD58 Antigens / metabolism
  • Humans
  • Immunity, Mucosal / genetics
  • Immunity, Mucosal / physiology
  • Immunologic Memory / genetics
  • Immunologic Memory / physiology*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Pancreas / immunology
  • Pancreas / metabolism*
  • Pancreas / pathology
  • Pancreatitis / genetics
  • Pancreatitis / immunology*
  • Pancreatitis / metabolism*
  • Programmed Cell Death 1 Receptor / genetics
  • Programmed Cell Death 1 Receptor / metabolism*
  • Signal Transduction
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism*

Substances

  • B7-H1 Antigen
  • CD274 protein, human
  • CD58 Antigens
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor