The Presence of HLA-E-Restricted, CMV-Specific CD8+ T Cells in the Blood of Lung Transplant Recipients Correlates with Chronic Allograft Rejection

PLoS One. 2015 Aug 24;10(8):e0135972. doi: 10.1371/journal.pone.0135972. eCollection 2015.

Abstract

The human cytomegalovirus (CMV) immune evasion protein, UL40, shares an identical peptide sequence with that found in the leader sequence of many human leukocyte antigen (HLA)-C alleles and when complexed with HLA-E, can modulate NK cell functions via interactions with the CD94-NKG2 receptors. However the UL40-derived sequence can also be immunogenic, eliciting robust CD8+ T cell responses. In the setting of solid organ transplantation these T cells may not only be involved in antiviral immunity but also can potentially contribute to allograft rejection when the UL40 epitope is also present in allograft-encoded HLA. Here we assessed 15 bilateral lung transplant recipients for the presence of HLA-E-restricted UL40 specific T cells by tetramer staining of peripheral blood mononuclear cells (PBMC). UL40-specific T cells were observed in 7 patients post-transplant however the magnitude of the response varied significantly between patients. Moreover, unlike healthy CMV seropositive individuals, longitudinal analyses revealed that proportions of such T cells fluctuated markedly. Nine patients experienced low-grade acute cellular rejection, of which 6 also demonstrated UL40-specific T cells. Furthermore, the presence of UL40-specific CD8+ T cells in the blood was significantly associated with allograft dysfunction, which manifested as Bronchiolitis Obliterans Syndrome (BOS). Therefore, this study suggests that minor histocompatibility antigens presented by HLA-E can represent an additional risk factor following lung transplantation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • CD8-Positive T-Lymphocytes / immunology
  • Cytomegalovirus / immunology
  • Cytomegalovirus / pathogenicity
  • Cytotoxicity, Immunologic*
  • Female
  • Graft Rejection / genetics
  • Graft Rejection / immunology
  • HLA-E Antigens
  • Histocompatibility Antigens Class I / blood
  • Histocompatibility Antigens Class I / immunology*
  • Humans
  • Killer Cells, Natural / immunology
  • Lung Transplantation / adverse effects*
  • Male
  • Middle Aged
  • NK Cell Lectin-Like Receptor Subfamily D / genetics
  • NK Cell Lectin-Like Receptor Subfamily D / immunology
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology
  • T-Lymphocytes, Cytotoxic / immunology*
  • Transplant Recipients
  • Viral Proteins / genetics
  • Viral Proteins / immunology

Substances

  • Histocompatibility Antigens Class I
  • NK Cell Lectin-Like Receptor Subfamily D
  • Receptors, Antigen, T-Cell
  • UL40 glycoprotein, Cytomegalovirus
  • Viral Proteins

Grants and funding

This work was supported by the National Health and Medical Research Council (nhmrc.gov.au) to AGB, Grant# APP1016629, the National Health and Medical Research Council (nhmrc.gov.au) to AGB, Grant# APP0509179, and the National Health and Medical Research Council (nhmrc.gov.au) to LCS, Grant# GNT0566571. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.