Single-nucleotide human disease mutation inactivates a blood-regenerative GATA2 enhancer

J Clin Invest. 2019 Mar 1;129(3):1180-1192. doi: 10.1172/JCI122694. Epub 2019 Feb 11.

Abstract

The development and function of stem and progenitor cells that produce blood cells are vital in physiology. GATA-binding protein 2 (GATA2) mutations cause GATA-2 deficiency syndrome involving immunodeficiency, myelodysplastic syndrome, and acute myeloid leukemia. GATA-2 physiological activities necessitate that it be strictly regulated, and cell type-specific enhancers fulfill this role. The +9.5 intronic enhancer harbors multiple conserved cis-elements, and germline mutations of these cis-elements are pathogenic in humans. Since mechanisms underlying how GATA2 enhancer disease mutations impact hematopoiesis and pathology are unclear, we generated mouse models of the enhancer mutations. While a multi-motif mutant was embryonically lethal, a single-nucleotide Ets motif mutant was viable, and steady-state hematopoiesis was normal. However, the Ets motif mutation abrogated stem/progenitor cell regeneration following stress. These results reveal a new mechanism in human genetics, in which a disease predisposition mutation inactivates enhancer regenerative activity, while sparing developmental activity. Mutational sensitization to stress that instigates hematopoietic failure constitutes a paradigm for GATA-2 deficiency syndrome and other contexts of GATA-2-dependent pathogenesis.

Keywords: Bone marrow differentiation; Hematology; Hematopoietic stem cells; Mouse models; Stem cells.

Publication types

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

MeSH terms

  • Animals
  • Enhancer Elements, Genetic*
  • GATA2 Deficiency* / genetics
  • GATA2 Deficiency* / metabolism
  • GATA2 Transcription Factor* / genetics
  • GATA2 Transcription Factor* / metabolism
  • Germ-Line Mutation*
  • Hematopoiesis / genetics*
  • Humans
  • Mice
  • Mice, Mutant Strains
  • Nucleotide Motifs*
  • Regeneration / genetics*

Substances

  • GATA2 Transcription Factor
  • Gata2 protein, mouse