CD40 induces PIR-A+ macrophages to promote chronic allograft rejection

Int Immunopharmacol. 2025 Mar 26:150:114274. doi: 10.1016/j.intimp.2025.114274. Epub 2025 Feb 15.

Abstract

Background: Chronic rejection is the leading cause of progressive allograft function decline. Studies have demonstrated that CD40-CD40L-induced paired immunoglobulin-like receptor-A (PIR-A) is the MHC-I receptor necessary for the specific memory response in macrophages of mice with chronic rejection. However, the underlying mechanisms remain unclear.

Methods: BALB/c mouse hearts were transplanted into C57BL/6, RelB-/- or LysMCrePirafl/fl mice, and a chronic rejection model was established by injecting CTLA-4-Ig. CD40-CD40L blockade in recipients by injecting anti-CD40L antibody. Allograft survival was monitored and histologically was assessed. Bone marrow-derived macrophages were treated with an anti-CD40 antibody. PIR-A expression was assessed via various methods in vivo and in vitro. Transcription factor expression levels were detected using RNA sequencing. DNA specifically bound to transcription factors was detected using ChIP-seq.

Results: CD40 and PIR-A were highly expressed and colocalized in macrophage-infiltrating allograft in the mouse model. CD40-CD40L blockade inhibited PIR-A expression and prolonged allograft survival. Conditional deletion of Pira in recipient's macrophages inhibited chronic rejection and promoted long-term allograft acceptance. Mechanistically, CD40 may activate transcription factor NF-κB2 translocation into the nucleus to up-regulate PIR-A expression, promoting chronic rejection of cardiac transplantation. NF-κB2 regulated PIR-A expression by binding to the intergenic region of Pira.

Conclusions: Our data suggest that Pira is a potential target to induce long-term allograft tolerance. CD40 may activate transcription factor NF-κB2 translocation into the nucleus to up-regulate PIR-A expression, promoting chronic rejection of cardiac transplantation. The study findings provide novel therapeutic opportunities to promote transplant survival in clinical settings.

Keywords: Allograft survival; CD40; Chronic rejection; NF-κB2; PIR-A.

MeSH terms

  • Allografts / immunology
  • Animals
  • CD40 Antigens* / genetics
  • CD40 Antigens* / immunology
  • CD40 Antigens* / metabolism
  • CD40 Ligand / immunology
  • Chronic Disease
  • Graft Rejection* / immunology
  • Graft Survival / immunology
  • Heart Transplantation*
  • Macrophages* / immunology
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Receptors, Immunologic* / genetics
  • Receptors, Immunologic* / immunology
  • Receptors, Immunologic* / metabolism
  • Transcription Factor RelB / genetics

Substances

  • CD40 Antigens
  • Receptors, Immunologic
  • CD40 Ligand
  • Transcription Factor RelB
  • Relb protein, mouse