Ablation of interferon regulatory factor 4 in T cells induces "memory" of transplant tolerance that is irreversible by immune checkpoint blockade

Am J Transplant. 2019 Mar;19(3):884-893. doi: 10.1111/ajt.15196. Epub 2018 Dec 25.

Abstract

Achieving transplant tolerance remains the ultimate goal in the field of organ transplantation. We demonstrated previously that ablation of the transcription factor interferon regulatory factor 4 (IRF4) in T cells induced heart transplant acceptance by driving allogeneic CD4+ T cell dysfunction. Herein, we showed that heart-transplanted mice with T cell-specific IRF4 deletion were tolerant to donor-specific antigens and accepted the subsequently transplanted donor-type but not third-party skin allografts. Moreover, despite the rejection of the primary heart grafts in T cell-specific Irf4 knockout mice under immune checkpoint blockade, the establishment of donor-specific tolerance in these mice was unhindered. By tracking alloantigen-specific CD4+ T cells in vivo, we revealed that checkpoint blockade restored the expression levels of the majority of wild-type T cell-expressed genes in Irf4-deficient T cells on day 6 post-heart grafting, indicating the initial reinvigoration of Irf4-deficient T cells. Nevertheless, checkpoint blockade did not restore cell frequency, effector memory cell generation, and IFN-γ/TNF-α production of Irf4-/- alloreactive T cells at day 30 post-heart grafting. Hence, targeting IRF4 represents a potential therapeutic strategy for driving intrinsic T cell dysfunction and achieving alloantigen-specific transplant tolerance.

Keywords: T cell biology; animal models: murine; basic (laboratory) research/science; cellular biology; graft survival; immunobiology; organ transplantation in general; tolerance.

Publication types

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

MeSH terms

  • Allografts
  • Animals
  • CD4-Positive T-Lymphocytes / immunology*
  • Gene Expression Regulation
  • Graft Rejection / prevention & control*
  • Graft Survival / immunology*
  • Heart Transplantation / methods*
  • Immunologic Memory / immunology*
  • Interferon Regulatory Factors / physiology*
  • Isoantigens / immunology
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • T-Lymphocytes, Regulatory / immunology
  • Tissue Donors
  • Transplantation Tolerance / immunology*

Substances

  • Interferon Regulatory Factors
  • Isoantigens
  • interferon regulatory factor-4