Enhanced PD-1 expression by T cells in cerebrospinal fluid does not reflect functional exhaustion during chronic human immunodeficiency virus type 1 infection

J Virol. 2010 Jan;84(1):131-40. doi: 10.1128/JVI.01181-09.

Abstract

During chronic viral infections, T cells are exhausted due to constant antigen exposure and are associated with enhanced programmed death 1 (PD-1) expression. Deficiencies in the PD-1/programmed death-ligand 1 (PD-L1) pathway are associated with autoimmune diseases, including those of the central nervous system (CNS). To understand the role of PD-1 expression in regulating T-cell immunity in the CNS during chronic infection, we characterized PD-1 expression in cerebrospinal fluid (CSF) and blood of individuals with chronic human immunodeficiency virus type 1 (HIV-1) infection. PD-1 expression was higher on HIV-specific CD8(+) T cells than on total CD8(+) T cells in both CSF and blood. PD-1 expression on CSF T cells correlated positively with CSF HIV-1 RNA and inversely with blood CD4(+) T-cell counts, suggesting that HIV-1 infection drives higher PD-1 expression on CSF T cells. However, in every HIV-positive individual, PD-1 expression was higher on T cells in CSF than on those in blood, despite HIV-1 RNA levels being lower. Among healthy HIV-negative controls, PD-1 expression was higher in CSF than in blood. Furthermore, frequencies of the senescence marker CD57 were lower on CSF T cells than on blood T cells, consistent with our prior observation of enhanced ex vivo functional capacity of CSF T cells. The higher PD-1 expression level on CSF T cells therefore does not reflect cellular exhaustion but may be a mechanism to downregulate immune-mediated tissue damage in the CNS. As inhibition of the PD-1/PD-L1 pathway is pursued as a therapeutic option for viral infections, potential effects of such a blockade on development of autoimmune responses in the CNS should be considered.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Antigens, CD / cerebrospinal fluid
  • Antigens, CD / genetics*
  • Apoptosis Regulatory Proteins / cerebrospinal fluid
  • Apoptosis Regulatory Proteins / genetics*
  • Blood Cells / immunology
  • CD4-Positive T-Lymphocytes / pathology
  • CD57 Antigens / analysis
  • CD8-Positive T-Lymphocytes / chemistry
  • CD8-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / virology
  • Case-Control Studies
  • Cellular Senescence
  • Central Nervous System / immunology
  • Cerebrospinal Fluid / immunology
  • Chronic Disease
  • Gene Expression Regulation / immunology*
  • HIV Infections / immunology*
  • Humans
  • Programmed Cell Death 1 Receptor
  • RNA, Viral / analysis
  • T-Lymphocytes / metabolism*
  • T-Lymphocytes / virology

Substances

  • Antigens, CD
  • Apoptosis Regulatory Proteins
  • CD57 Antigens
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor
  • RNA, Viral