Molecular mechanisms of bleeding disorderassociated GFI1BQ287* mutation and its affected pathways in megakaryocytes and platelets

Haematologica. 2019 Jul;104(7):1460-1472. doi: 10.3324/haematol.2018.194555. Epub 2019 Jan 17.

Abstract

Dominant-negative mutations in the transcription factor Growth Factor Independence-1B (GFI1B), such as GFI1BQ287*, cause a bleeding disorder characterized by a plethora of megakaryocyte and platelet abnormalities. The deregulated molecular mechanisms and pathways are unknown. Here we show that both normal and Q287* mutant GFI1B interacted most strongly with the lysine specific demethylase-1 - REST corepressor - histone deacetylase (LSD1-RCOR-HDAC) complex in megakaryoblasts. Sequestration of this complex by GFI1BQ287* and chemical separation of GFI1B from LSD1 induced abnormalities in normal megakaryocytes comparable to those seen in patients. Megakaryocytes derived from GFI1BQ287*-induced pluripotent stem cells also phenocopied abnormalities seen in patients. Proteome studies on normal and mutant-induced pluripotent stem cell-derived megakaryocytes identified a multitude of deregulated pathways downstream of GFI1BQ287* including cell division and interferon signaling. Proteome studies on platelets from GFI1BQ287* patients showed reduced expression of proteins implicated in platelet function, and elevated expression of proteins normally downregulated during megakaryocyte differentiation. Thus, GFI1B and LSD1 regulate a broad developmental program during megakaryopoiesis, and GFI1BQ287* deregulates this program through LSD1-RCOR-HDAC sequestering.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Blood Coagulation Disorders / genetics
  • Blood Coagulation Disorders / metabolism
  • Blood Coagulation Disorders / pathology*
  • Blood Platelets / metabolism
  • Blood Platelets / pathology*
  • Cell Differentiation
  • Co-Repressor Proteins / genetics
  • Co-Repressor Proteins / metabolism
  • Gene Expression Regulation*
  • Histone Deacetylase 1 / genetics
  • Histone Deacetylase 1 / metabolism
  • Histone Deacetylase 2 / genetics
  • Histone Deacetylase 2 / metabolism
  • Histone Demethylases / genetics
  • Histone Demethylases / metabolism
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Induced Pluripotent Stem Cells / pathology*
  • Megakaryocytes / metabolism
  • Megakaryocytes / pathology*
  • Mutation*
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Phenotype
  • Protein Interaction Maps
  • Proteome / analysis
  • Proto-Oncogene Proteins / genetics*
  • Proto-Oncogene Proteins / metabolism
  • Repressor Proteins / genetics*
  • Repressor Proteins / metabolism

Substances

  • Co-Repressor Proteins
  • GFI1B protein, human
  • Nerve Tissue Proteins
  • Proteome
  • Proto-Oncogene Proteins
  • RCOR1 protein, human
  • Repressor Proteins
  • Histone Demethylases
  • KDM1A protein, human
  • HDAC1 protein, human
  • HDAC2 protein, human
  • Histone Deacetylase 1
  • Histone Deacetylase 2