Prevalence of polyreactive innate clones among graft--infiltrating B cells in human cardiac allograft vasculopathy

J Heart Lung Transplant. 2018 Mar;37(3):385-393. doi: 10.1016/j.healun.2017.09.011. Epub 2017 Sep 28.

Abstract

Background: Cardiac allograft vasculopathy (CAV) has been associated with graft-infiltrating B cells, although their characteristics are still unclear. In this study we examined the frequency, localization and reactivity profile of graft-infiltrating B cells to determine their contribution to the pathophysiology of CAV.

Methods: B cells, plasma cells and macrophages were examined by immunohistochemistry in 56 allografts with CAV, 49 native failed hearts and 25 autopsy specimens. A total of 102 B-cell clones were immortalized directly from the infiltrates of 3 fresh cardiac samples with CAV. Their secreted antibodies were assessed using enzyme-linked immunoassay and flow cytometry.

Results: B-cell infiltration was observed around coronary arteries in 93% of allograft explants with CAV. Comparatively, intragraft B cells were less frequent and less dense in the intraventricular myocardium from where routine biopsies are obtained. Plasma cells and macrophages were also detected in 85% and 95% of explants, respectively. Remarkably, B-cell infiltrates were not associated with circulating donor-specific antibodies (DSA) or prior episodes of antibody-mediated rejection (AMR). Among all B-cell clones generated from 3 explants with CAV, a majority secreted natural antibodies reactive to multiple autoantigens and apoptotic cells, a characteristic of innate B cells.

Conclusions: Our study reveals a high frequency of infiltrating B cells around the coronary arteries of allografts with CAV, independent of DSA or AMR. These cells are enriched for innate B cells with a polyreactive profile. The findings shift the focus from conventional DSA-producing B cells to the potentially pathogenic polyreactive B cells in the development of clinical CAV.

Keywords: autoantibodies; cardiac allograft vasculopathy; graft-infiltrating B cells; innate B cells; polyreactive B cells.

Publication types

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

MeSH terms

  • Adult
  • Allografts
  • B-Lymphocytes*
  • Coronary Artery Disease / blood*
  • Coronary Artery Disease / immunology*
  • Coronary Artery Disease / pathology
  • Coronary Vessels / pathology
  • Female
  • Heart Transplantation*
  • Humans
  • Immunohistochemistry
  • Macrophages
  • Male
  • Middle Aged
  • Plasma Cells
  • Postoperative Complications / blood*
  • Postoperative Complications / immunology*
  • Postoperative Complications / pathology
  • Young Adult