Substantive Similarities Between Synovial Fluid and Synovial Tissue T cells in Inflammatory Arthritis Via Single-Cell RNA and T Cell Receptor Sequencing

Arthritis Rheumatol. 2024 Nov;76(11):1594-1601. doi: 10.1002/art.42949. Epub 2024 Aug 27.

Abstract

Objective: Synovial fluid (SF)-derived T cells are frequently studied as a proxy for investigating the synovial tissue (ST) T cell infiltrate in inflammatory arthritis. However, because ST is the primary site of inflammatory activity, there is debate as to whether SF provides a true reflection of the ST T cell population.

Methods: In this study, we used single-cell RNA sequencing paired with single-cell T cell receptor (TCR) sequencing to directly compare memory T cells from paired samples of SF and ST from six patients with inflammatory arthritis to investigate their similarity in terms of TCR repertoire and T cell subset composition.

Results: The TCR repertoires of SF and ST T cells were strikingly similar, particularly for CD8+ T cells. A median of 49% of the total CD8+ TCR repertoire in SF was shared with ST, compared with 20% shared with blood. Similarly, 47% of the ST CD8+ TCR repertoire was shared with SF compared to 25% with blood. Furthermore, once the effect of collagenase digestion on gene expression by ST T cells had been accounted for, the frequencies of specific CD8+ and CD4+ T cell subsets were, in general, similar in SF and ST and were distinct from blood.

Conclusion: Our results suggest that T cells migrate and equilibrate between the SF and ST and maintain similar phenotypes in both sites. We conclude that SF is an appropriate proxy for investigating the T cell infiltrate in inflamed synovium, particularly in terms of investigating the TCR repertoire.

MeSH terms

  • Arthritis, Rheumatoid / genetics
  • Arthritis, Rheumatoid / immunology
  • CD8-Positive T-Lymphocytes* / immunology
  • Female
  • Humans
  • Male
  • Memory T Cells / immunology
  • Middle Aged
  • Receptors, Antigen, T-Cell* / genetics
  • Receptors, Antigen, T-Cell* / immunology
  • Sequence Analysis, RNA*
  • Single-Cell Analysis*
  • Synovial Fluid* / cytology
  • Synovial Fluid* / immunology
  • Synovial Membrane* / immunology
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocytes / immunology

Substances

  • Receptors, Antigen, T-Cell