KLF13 promotes SLE pathogenesis by modifying chromatin accessibility of key proinflammatory cytokine genes

Commun Biol. 2024 Nov 6;7(1):1446. doi: 10.1038/s42003-024-07099-0.

Abstract

Although significant progress has been achieved in elucidating the genetic architecture of systemic lupus erythematosus (SLE), identifying genes underlying the pathogenesis has been challenging. The NZM2410-derived lupus susceptibility Sle3 locus is associated with T cell hyperactivity and activated myeloid cells. However, candidate genes associated with these phenotypes have not been identified. Here, we narrow the Sle3 locus to a smaller genomic segment (Sle3k) and show that mice carrying Sle3k and Sle1 loci developed lupus nephritis. We identify Klf13 as the primary candidate gene that is associated with genome-wide transcription changes resulting in higher levels of proinflammatory cytokines, enhanced T cell activation, and hyperresponsiveness of myeloid cells. Correspondingly, Klf13 -/- mice display repression of genes involved in mediating immune activation, including key proinflammatory cytokines/chemokines in T cells and dysregulation in cytokine signaling pathways in myeloid cells in response to toll receptor ligands. Klf13 upregulation is associated with increased production of RANTES, a key chemokine in lupus nephritis, in activated T cells and the kidneys of lupus-prone mice. In sum, our findings reveal Klf13 as a key gene in the Sle3 interval in mediating lupus pathogenesis that may have implications in the rational design of new therapies for SLE.

MeSH terms

  • Animals
  • Cell Cycle Proteins
  • Chemokine CCL5 / genetics
  • Chemokine CCL5 / metabolism
  • Chromatin* / genetics
  • Chromatin* / metabolism
  • Cytokines* / genetics
  • Cytokines* / metabolism
  • Female
  • Genetic Predisposition to Disease
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism
  • Lupus Erythematosus, Systemic* / genetics
  • Lupus Erythematosus, Systemic* / immunology
  • Lupus Erythematosus, Systemic* / metabolism
  • Lupus Nephritis / genetics
  • Lupus Nephritis / immunology
  • Lupus Nephritis / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Myeloid Cells / metabolism
  • Repressor Proteins
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism

Substances

  • Cytokines
  • Chromatin
  • Klf13 protein, mouse
  • Kruppel-Like Transcription Factors
  • Chemokine CCL5
  • Repressor Proteins
  • Cell Cycle Proteins