Clonal hematopoiesis-related mutant ASXL1 promotes atherosclerosis in mice via dysregulated innate immunity

Nat Cardiovasc Res. 2024 Dec;3(12):1568-1583. doi: 10.1038/s44161-024-00579-w. Epub 2024 Dec 9.

Abstract

Certain somatic mutations provide a fitness advantage to hematopoietic stem cells and lead to clonal expansion of mutant blood cells, known as clonal hematopoiesis (CH). Among the most common CH mutations, ASXL1 mutations pose the highest risk for cardiovascular diseases (CVDs), yet the mechanisms by which they contribute to CVDs are unclear. Here we show that hematopoietic cells harboring C-terminally truncated ASXL1 mutant (ASXL1-MT) accelerate the development of atherosclerosis in Ldlr-/- mice. Transcriptome analyses of plaque cells showed that monocytes and macrophages expressing ASXL1-MT exhibit inflammatory signatures. Mechanistically, we demonstrate that wild-type ASXL1 has an unexpected non-epigenetic role by suppressing innate immune signaling through the inhibition of IRAK1-TAK1 interaction in the cytoplasm. This regulatory function is lost in ASXL1-MT, resulting in NF-κB activation. Inhibition of IRAK1/4 alleviated atherosclerosis driven by ASXL1-MT and decreased inflammatory monocytes. The present work provides a mechanistic and cellular explanation linking ASXL1 mutations, CH and CVDs.

MeSH terms

  • Animals
  • Aortic Diseases / genetics
  • Aortic Diseases / immunology
  • Aortic Diseases / pathology
  • Atherosclerosis* / genetics
  • Atherosclerosis* / immunology
  • Atherosclerosis* / metabolism
  • Atherosclerosis* / pathology
  • Clonal Hematopoiesis* / genetics
  • Disease Models, Animal*
  • Humans
  • Immunity, Innate* / genetics
  • Interleukin-1 Receptor-Associated Kinases* / genetics
  • Interleukin-1 Receptor-Associated Kinases* / metabolism
  • MAP Kinase Kinase Kinases / genetics
  • MAP Kinase Kinase Kinases / metabolism
  • Macrophages / immunology
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Monocytes / immunology
  • Monocytes / metabolism
  • Mutation*
  • NF-kappa B / genetics
  • NF-kappa B / metabolism
  • Plaque, Atherosclerotic / genetics
  • Plaque, Atherosclerotic / immunology
  • Plaque, Atherosclerotic / pathology
  • Repressor Proteins* / genetics
  • Repressor Proteins* / metabolism
  • Signal Transduction* / genetics

Substances

  • Repressor Proteins
  • Interleukin-1 Receptor-Associated Kinases
  • Asxl1 protein, mouse
  • Irak1 protein, mouse
  • MAP kinase kinase kinase 7
  • MAP Kinase Kinase Kinases
  • NF-kappa B