Heterologous Cytomegalovirus and Allo-Reactivity by Shared T Cell Receptor Repertoire in Kidney Transplantation

Front Immunol. 2019 Oct 31:10:2549. doi: 10.3389/fimmu.2019.02549. eCollection 2019.

Abstract

Cytomegalovirus (CMV) infection is associated with allograft rejection but the mechanisms behind are poorly defined yet. Although cross-reactivity of T cells to alloantigen and CMV has been hypothesized, direct evidence in patients is lacking. In this observational cohort study, we tested the pre-transplant effector/memory T cell response to CMV peptide pools and alloantigen in 78 living donor/recipient pairs using the interferon-gamma Enzyme-Linked ImmunoSpot (ELISPOT) assay. To prove the hypothesis of cross-reactivity, we analyzed by applying next-generation sequencing the T cell receptor ß (TCR- ß) repertoire of CMV- and alloantigen-reactive T cells enriched from peripheral pre-transplant blood of 11 CMV-seropositive and HLA class I mismatched patients. Moreover, the TCR-repertoire was also analyzed in the allograft biopsies of those patients. There was a significant association between the presence of pre-transplant CMV immediate-early protein 1 (IE-1)-specific effector/memory T cells and acute renal allograft rejection and function (p = 0.01). Most importantly, we revealed shared TCR-ß sequences between CMV-IE1 and donor alloantigen-reactive T cells in all pre-transplant peripheral blood samples analyzed in CMV-seropositive patients who received HLA class I mismatched grafts. Identical TCR sequences were also found in particular in post-transplant allograft biopsies of patients with concomitant CMV infection and rejection. Our data show the presence of functional, cross-reactive T cells and their clonotypes in peripheral blood and in kidney allograft tissue. It is therefore likely that CMV-donor cross-reactivity as well as CMV specific T cell elicited inflammation is involved in the processes that affect allograft outcomes.

Keywords: ELISPOT; TCR repertoire; cross-reactivity; cytomegalovirus; heterologous immunity; kidney transplantation; rejection.

Publication types

  • Clinical Trial
  • Observational Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Allografts
  • Biopsy
  • Cohort Studies
  • Cytomegalovirus / immunology*
  • Cytomegalovirus Infections* / etiology
  • Cytomegalovirus Infections* / genetics
  • Cytomegalovirus Infections* / immunology
  • Cytomegalovirus Infections* / pathology
  • Female
  • Humans
  • Immunologic Memory*
  • Isoantigens / genetics
  • Isoantigens / immunology
  • Kidney Transplantation*
  • Male
  • Middle Aged
  • Receptors, Antigen, T-Cell, alpha-beta* / immunology
  • T-Lymphocytes* / microbiology
  • T-Lymphocytes* / pathology

Substances

  • Isoantigens
  • Receptors, Antigen, T-Cell, alpha-beta