Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF

Nat Med. 2010 Oct;16(10):1147-51. doi: 10.1038/nm.2232. Epub 2010 Oct 3.

Abstract

CD8(+) T cells in chronic viral infections such as HIV develop functional defects including loss of interleukin-2 (IL-2) secretion and decreased proliferative potential that are collectively termed 'exhaustion'. Exhausted T cells express increased amounts of multiple inhibitory receptors, such as programmed death-1 (PD-1), that contribute to impaired virus-specific T cell function. Although reversing PD-1 inhibition is therefore an attractive therapeutic strategy, the cellular mechanisms by which PD-1 ligation results in T cell inhibition are not fully understood. PD-1 is thought to limit T cell activation by attenuating T cell receptor (TCR) signaling. It is not known whether PD-1 also acts by upregulating genes in exhausted T cells that impair their function. Here we analyzed gene expression profiles from HIV-specific CD8(+) T cells in individuals with HIV and show that PD-1 coordinately upregulates a program of genes in exhausted CD8(+) T cells from humans and mice. This program includes upregulation of basic leucine transcription factor, ATF-like (BATF), a transcription factor in the AP-1 family. Enforced expression of BATF was sufficient to impair T cell proliferation and cytokine secretion, whereas BATF knockdown reduced PD-1 inhibition. Silencing BATF in T cells from individuals with chronic viremia rescued HIV-specific T cell function. Thus, inhibitory receptors can cause T cell exhaustion by upregulating genes--such as BATF--that inhibit T cell function. Such genes may provide new therapeutic opportunities to improve T cell immunity to HIV.

Publication types

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

MeSH terms

  • Animals
  • Antigens, CD / physiology*
  • Apoptosis Regulatory Proteins / physiology*
  • Basic-Leucine Zipper Transcription Factors / genetics*
  • CD8-Positive T-Lymphocytes / metabolism*
  • Gene Expression Profiling*
  • Gene Expression Regulation
  • HIV / immunology*
  • Humans
  • Interferon-gamma / biosynthesis
  • Interleukin-2 / biosynthesis
  • Lymphocytic Choriomeningitis / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Programmed Cell Death 1 Receptor
  • T-Lymphocytes / physiology*

Substances

  • Antigens, CD
  • Apoptosis Regulatory Proteins
  • BATF protein, human
  • Basic-Leucine Zipper Transcription Factors
  • Batf protein, mouse
  • Interleukin-2
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor
  • Interferon-gamma

Associated data

  • GEO/GSE24082