Sumoylation of CCAAT/enhancer-binding protein α promotes the biased primitive hematopoiesis of zebrafish

Blood. 2011 Jun 30;117(26):7014-20. doi: 10.1182/blood-2010-12-325712. Epub 2011 May 19.

Abstract

Hematopoiesis is evolutionarily conserved from zebrafish to mammals, and this includes both primitive and definitive waves during embryogenesis. Primitive hematopoiesis is dominated by erythropoiesis with limited myelopoiesis. Protein sumoylation, a ubiquitination-like posttranslational protein modification, is implicated in a variety of biochemical processes, most notably in transcriptional repression. We show here that the loss of 6 small ubiquitin-related modifier (SUMO) paralogs triggers a sharp up-regulation of the myeloid-specific marker mpo and down-regulation of the erythroid-specific marker gata1 in myelo-erythroid progenitor cells (MPCs) in the intermediate cell mass (ICM) during primitive hematopoiesis. Accordingly, in transgenic zebrafish lines, hyposumoylation expands myelopoiesis at the expense of erythropoiesis. A SUMO-CCAAT/enhancer-binding protein α (SUMO-C/ebpα) fusion restores the normal myelopoiesis/erythropoiesis balance, suggesting that sumoylation status of C/ebpα contributes to myelo-erythroid lineage determination. Our results therefore implicate sumoylation in early lineage determination and reveal the possible molecular mechanism underlying the puzzling biased primitive hematopoiesis in vertebrates.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • CCAAT-Enhancer-Binding Protein-alpha / genetics
  • CCAAT-Enhancer-Binding Protein-alpha / physiology*
  • Cell Line
  • Cell Lineage
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / metabolism*
  • GATA1 Transcription Factor / genetics
  • GATA1 Transcription Factor / metabolism
  • Gene Silencing
  • Genes, Reporter
  • Hematopoiesis, Extramedullary*
  • Humans
  • Mesoderm
  • Myeloid Progenitor Cells
  • Myelopoiesis
  • Peroxidase / genetics
  • Peroxidase / metabolism
  • Protein Isoforms / antagonists & inhibitors
  • Protein Isoforms / genetics
  • Protein Isoforms / physiology
  • Recombinant Fusion Proteins
  • Small Ubiquitin-Related Modifier Proteins / antagonists & inhibitors
  • Small Ubiquitin-Related Modifier Proteins / genetics
  • Small Ubiquitin-Related Modifier Proteins / metabolism*
  • Sumoylation*
  • Up-Regulation*
  • Zebrafish
  • Zebrafish Proteins / antagonists & inhibitors
  • Zebrafish Proteins / genetics
  • Zebrafish Proteins / metabolism
  • Zebrafish Proteins / physiology*

Substances

  • CCAAT-Enhancer-Binding Protein-alpha
  • GATA1 Transcription Factor
  • Protein Isoforms
  • Recombinant Fusion Proteins
  • Small Ubiquitin-Related Modifier Proteins
  • Zebrafish Proteins
  • gata1a protein, zebrafish
  • Peroxidase