Single cell RNA-sequencing delineates CD8+ tissue resident memory T cells maintaining rejection in liver transplantation

Theranostics. 2024 Aug 12;14(12):4844-4860. doi: 10.7150/thno.96928. eCollection 2024.

Abstract

Rationale: Understanding the immune mechanisms associated with liver transplantation (LT), particularly the involvement of tissue-resident memory T cells (TRMs), represents a significant challenge. Methods: This study employs a multi-omics approach to analyse liver transplant samples from both human (n = 17) and mouse (n = 16), utilizing single-cell RNA sequencing, bulk RNA sequencing, and immunological techniques. Results: Our findings reveal a comprehensive T cell-centric landscape in LT across human and mouse species, involving 235,116 cells. Notably, we found a substantial increase in CD8+ TRMs within rejected grafts compared to stable ones. The elevated presence of CD8+ TRMs is characterised by a distinct expression profile, featuring upregulation of tissue-residency markers (CD69, CXCR6, CD49A and CD103+/-,), immune checkpoints (PD1, CTLA4, and TIGIT), cytotoxic markers (GZMB and IFNG) and proliferative markers (PCNA and TOP2A) during rejection. Furthermore, there is a high expression of transcription factors such as EOMES and RUNX3. Functional assays and analyses of cellular communication underscore the active role of CD8+ TRMs in interacting with other tissue-resident cells, particularly Kupffer cells, especially during rejection episodes. Conclusions: These insights into the distinctive activation and interaction patterns of CD8+ TRMs suggest their potential utility as biomarkers for graft rejection, paving the way for novel therapeutic strategies aimed at enhancing graft tolerance and improving overall transplant outcomes.

Keywords: graft rejection; immune tolerance; liver transplantation; multi-omics; tissue-resident memory T cells.

MeSH terms

  • Animals
  • Antigens, CD / genetics
  • Antigens, CD / metabolism
  • CD8-Positive T-Lymphocytes* / immunology
  • CD8-Positive T-Lymphocytes* / metabolism
  • Core Binding Factor Alpha 3 Subunit / genetics
  • Core Binding Factor Alpha 3 Subunit / metabolism
  • Female
  • Graft Rejection* / immunology
  • Humans
  • Immunologic Memory
  • Liver Transplantation*
  • Male
  • Memory T Cells* / immunology
  • Memory T Cells* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • Sequence Analysis, RNA / methods
  • Single-Cell Analysis* / methods
  • T-Box Domain Proteins

Substances

  • Core Binding Factor Alpha 3 Subunit
  • Runx3 protein, human
  • EOMES protein, human
  • Antigens, CD
  • Runx3 protein, mouse
  • T-Box Domain Proteins