Mutant U2AF1-induced alternative splicing of H2afy (macroH2A1) regulates B-lymphopoiesis in mice

Cell Rep. 2021 Aug 31;36(9):109626. doi: 10.1016/j.celrep.2021.109626.

Abstract

Somatic mutations in spliceosome genes are found in ∼50% of patients with myelodysplastic syndromes (MDS), a myeloid malignancy associated with low blood counts. Expression of the mutant splicing factor U2AF1(S34F) alters hematopoiesis and mRNA splicing in mice. Our understanding of the functionally relevant alternatively spliced target genes that cause hematopoietic phenotypes in vivo remains incomplete. Here, we demonstrate that reduced expression of H2afy1.1, an alternatively spliced isoform of the histone H2A variant gene H2afy, is responsible for reduced B cells in U2AF1(S34F) mice. Deletion of H2afy or expression of U2AF1(S34F) reduces expression of Ebf1 (early B cell factor 1), a key transcription factor for B cell development, and mechanistically, H2AFY is enriched at the EBF1 promoter. Induced expression of H2AFY1.1 in U2AF1(S34F) cells rescues reduced EBF1 expression and B cells numbers in vivo. Collectively, our data implicate alternative splicing of H2AFY as a contributor to lymphopenia induced by U2AF1(S34F) in mice and MDS.

Keywords: B-lymphopoiesis; EBF1; H2AFY; U2AF1; U2AF1(S34F); alternative splicing; hematopoiesis; macroH2A1; myelodysplastic syndromes; spliceosome gene mutations.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alternative Splicing*
  • Animals
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism*
  • Binding Sites
  • Case-Control Studies
  • HEK293 Cells
  • Histones / genetics
  • Histones / metabolism*
  • Humans
  • K562 Cells
  • Lymphopoiesis*
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mutation
  • Myelodysplastic Syndromes / genetics
  • Myelodysplastic Syndromes / immunology
  • Myelodysplastic Syndromes / metabolism*
  • Promoter Regions, Genetic
  • Signal Transduction
  • Splicing Factor U2AF / genetics
  • Splicing Factor U2AF / metabolism*
  • Trans-Activators / genetics
  • Trans-Activators / metabolism

Substances

  • Ebf1 protein, mouse
  • Histones
  • MACROH2A2 protein, human
  • Macroh2a1 protein, mouse
  • Splicing Factor U2AF
  • Trans-Activators
  • U2AF1 protein, human
  • Zrsr1 protein, mouse