CD4+CD57+ senescent T cells as promoters of systemic lupus erythematosus pathogenesis and the therapeutic potential of senolytic BCL-2 inhibitor

Eur J Immunol. 2024 Jul;54(7):e2350603. doi: 10.1002/eji.202350603. Epub 2024 May 16.

Abstract

Systemic lupus erythematosus (SLE) is a complex autoimmune disease characterized by persistent activation of immune cells and overproduction of autoantibodies. The accumulation of senescent T and B cells has been observed in SLE and other immune-mediated diseases. However, the exact mechanistic pathways contributing to this process in SLE remain incompletely understood. In this study, we found that in SLE patients: (1) the frequency of CD4+CD57+ senescent T cells was significantly elevated and positively correlated with disease activity; (2) the expression levels of B-lymphoma-2 (BCL-2) family and interferon-induced genes (ISGs) were significantly upregulated; and (3) in vitro, the cytokine IL-15 stimulation increased the frequency of senescent CD4+ T cells and upregulated the expression of BCL-2 family and ISGs. Further, treatment with ABT-263 (a senolytic BCL-2 inhibitor) in MRL/lpr mice resulted in decreased: (1) frequency of CD4+CD44hiCD62L-PD-1+CD153+ senescent CD4+ T cells; (2) frequency of CD19+CD11c+T-bet+ age-related B cells; (3) level of serum antinuclear antibody; (4) proteinuria; (5) frequency of Tfh cells; and (6) renal histopathological abnormalities. Collectively, these results indicated a dominant role for CD4+CD57+ senescent CD4+ T cells in the pathogenesis of SLE and senolytic BCL-2 inhibitor ABT-263 may be the potential treatment in ameliorating lupus phenotypes.

Keywords: CD4+ T cell; CD57; cellular senescence; senolytics; systemic lupus erythematosus.

MeSH terms

  • Adult
  • Aniline Compounds / pharmacology
  • Aniline Compounds / therapeutic use
  • Animals
  • CD4-Positive T-Lymphocytes* / immunology
  • Cellular Senescence* / drug effects
  • Cellular Senescence* / immunology
  • Female
  • Humans
  • Lupus Erythematosus, Systemic* / drug therapy
  • Lupus Erythematosus, Systemic* / immunology
  • Male
  • Mice
  • Mice, Inbred MRL lpr
  • Middle Aged
  • Proto-Oncogene Proteins c-bcl-2* / antagonists & inhibitors
  • Proto-Oncogene Proteins c-bcl-2* / genetics
  • Proto-Oncogene Proteins c-bcl-2* / metabolism
  • Senotherapeutics / pharmacology
  • Sulfonamides* / pharmacology

Substances

  • Proto-Oncogene Proteins c-bcl-2
  • navitoclax
  • Sulfonamides
  • Aniline Compounds
  • Senotherapeutics