Exhaustion of bacteria-specific CD4 T cells and microbial translocation in common variable immunodeficiency disorders

J Exp Med. 2014 Sep 22;211(10):2033-45. doi: 10.1084/jem.20140039. Epub 2014 Sep 15.

Abstract

In the present study, we have investigated the functional profile of CD4 T cells from patients with common variable immunodeficiency (CVID), including production of cytokines and proliferation in response to bacteria and virus-derived antigens. We show that the functional impairment of CD4 T cells, including the reduced capacity to proliferate and to produce IFN-γ and IL-2, was restricted to bacteria-specific and not virus-specific CD4 T cells. High levels of endotoxins were found in the plasma of patients with CVID, suggesting that CD4 T cell dysfunction might be caused by bacterial translocation. Of note, endotoxemia was associated with significantly higher expression of programmed death 1 (PD-1) on CD4 T cells. The blockade of the PD-1-PD-L1/2 axis in vitro restored CD4 T cell proliferation capacity, thus indicating that PD-1 signaling negatively regulates CD4 T cell functions. Finally, we showed that intravenous immunoglobulin G (IVIG) treatment significantly reduced endotoxemia and the percentage of PD-1(+) CD4 T cells, and restored bacteria-specific CD4 T cell cytokine production and proliferation. In conclusion, the present study demonstrates that the CD4 T cell exhaustion and functional impairment observed in CVID patients is associated with bacterial translocation and that IVIG treatment resolves bacterial translocation and restores CD4 T cell functions.

MeSH terms

  • Administration, Intravenous
  • Analysis of Variance
  • Antigens, Bacterial / immunology
  • Antigens, Viral / immunology
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / microbiology
  • Common Variable Immunodeficiency / immunology*
  • Common Variable Immunodeficiency / microbiology
  • Cytokines / immunology
  • Flow Cytometry
  • Humans
  • Immunoglobulin G / administration & dosage
  • Immunoglobulin G / pharmacology
  • Leukocytes, Mononuclear / immunology
  • Limulus Test
  • Programmed Cell Death 1 Receptor / immunology*
  • Programmed Cell Death 1 Receptor / metabolism
  • Signal Transduction / immunology*

Substances

  • Antigens, Bacterial
  • Antigens, Viral
  • Cytokines
  • Immunoglobulin G
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor