STAG2 mutations reshape the cohesin-structured spatial chromatin architecture to drive gene regulation in acute myeloid leukemia

Cell Rep. 2024 Aug 27;43(8):114498. doi: 10.1016/j.celrep.2024.114498. Epub 2024 Jul 30.

Abstract

Cohesin shapes the chromatin architecture, including enhancer-promoter interactions. Its components, especially STAG2, but not its paralog STAG1, are frequently mutated in myeloid malignancies. To elucidate the underlying mechanisms of leukemogenesis, we comprehensively characterized genetic, transcriptional, and chromatin conformational changes in acute myeloid leukemia (AML) patient samples. Specific loci displayed altered cohesin occupancy, gene expression, and local chromatin activation, which were not compensated by the remaining STAG1-cohesin. These changes could be linked to disrupted spatial chromatin looping in cohesin-mutated AMLs. Complementary depletion of STAG2 or STAG1 in primary human hematopoietic progenitors (HSPCs) revealed effects resembling STAG2-mutant AML-specific changes following STAG2 knockdown, not invoked by the depletion of STAG1. STAG2-deficient HSPCs displayed impaired differentiation capacity and maintained HSPC-like gene expression. This work establishes STAG2 as a key regulator of chromatin contacts, gene expression, and differentiation in the hematopoietic system and identifies candidate target genes that may be implicated in human leukemogenesis.

Keywords: CP: Cancer; CP: Molecular biology; Hi-C; RAD21; STAG2; acute myeloid leukemia; cohesin mutations; epigenetics; gene regulation; hematopoiesis; hematopoietic stem and progenitor cells; spatial chromatin structure.

MeSH terms

  • Antigens, Nuclear / genetics
  • Antigens, Nuclear / metabolism
  • Cell Cycle Proteins* / genetics
  • Cell Cycle Proteins* / metabolism
  • Cell Differentiation / genetics
  • Chromatin* / metabolism
  • Chromosomal Proteins, Non-Histone* / genetics
  • Chromosomal Proteins, Non-Histone* / metabolism
  • Cohesins*
  • Gene Expression Regulation, Leukemic
  • Hematopoietic Stem Cells / metabolism
  • Humans
  • Leukemia, Myeloid, Acute* / genetics
  • Leukemia, Myeloid, Acute* / metabolism
  • Leukemia, Myeloid, Acute* / pathology
  • Mutation* / genetics
  • Nuclear Proteins

Substances

  • Cohesins
  • Cell Cycle Proteins
  • STAG2 protein, human
  • Chromatin
  • Chromosomal Proteins, Non-Histone
  • STAG1 protein, human
  • Antigens, Nuclear
  • Nuclear Proteins