Divergent functions of hematopoietic transcription factors in lineage priming and differentiation during erythro-megakaryopoiesis

Genome Res. 2014 Dec;24(12):1932-44. doi: 10.1101/gr.164178.113. Epub 2014 Oct 15.

Abstract

Combinatorial actions of relatively few transcription factors control hematopoietic differentiation. To investigate this process in erythro-megakaryopoiesis, we correlated the genome-wide chromatin occupancy signatures of four master hematopoietic transcription factors (GATA1, GATA2, TAL1, and FLI1) and three diagnostic histone modification marks with the gene expression changes that occur during development of primary cultured megakaryocytes (MEG) and primary erythroblasts (ERY) from murine fetal liver hematopoietic stem/progenitor cells. We identified a robust, genome-wide mechanism of MEG-specific lineage priming by a previously described stem/progenitor cell-expressed transcription factor heptad (GATA2, LYL1, TAL1, FLI1, ERG, RUNX1, LMO2) binding to MEG-associated cis-regulatory modules (CRMs) in multipotential progenitors. This is followed by genome-wide GATA factor switching that mediates further induction of MEG-specific genes following lineage commitment. Interaction between GATA and ETS factors appears to be a key determinant of these processes. In contrast, ERY-specific lineage priming is biased toward GATA2-independent mechanisms. In addition to its role in MEG lineage priming, GATA2 plays an extensive role in late megakaryopoiesis as a transcriptional repressor at loci defined by a specific DNA signature. Our findings reveal important new insights into how ERY and MEG lineages arise from a common bipotential progenitor via overlapping and divergent functions of shared hematopoietic transcription factors.

Publication types

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

MeSH terms

  • Animals
  • Base Sequence
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Binding Sites
  • Cell Differentiation*
  • Cell Lineage*
  • Chromatin / genetics
  • Chromatin / metabolism
  • Cluster Analysis
  • Erythropoiesis / physiology*
  • GATA1 Transcription Factor / metabolism
  • GATA2 Transcription Factor / metabolism
  • Gene Expression Profiling
  • Gene Silencing
  • Genome-Wide Association Study
  • Hematopoietic Stem Cells / cytology*
  • Hematopoietic Stem Cells / metabolism*
  • Histones / metabolism
  • Mice
  • Models, Biological
  • Nucleotide Motifs
  • Protein Binding
  • Proto-Oncogene Protein c-fli-1 / metabolism
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-ets / metabolism
  • T-Cell Acute Lymphocytic Leukemia Protein 1
  • Thrombopoiesis / physiology*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transcription, Genetic

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Chromatin
  • GATA1 Transcription Factor
  • GATA2 Transcription Factor
  • Histones
  • Proto-Oncogene Protein c-fli-1
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-ets
  • T-Cell Acute Lymphocytic Leukemia Protein 1
  • Tal1 protein, mouse
  • Transcription Factors

Associated data

  • GEO/GSE49664