Aberrant ZNF423 impedes B cell differentiation and is linked to adverse outcome of ETV6-RUNX1 negative B precursor acute lymphoblastic leukemia

J Exp Med. 2013 Oct 21;210(11):2289-304. doi: 10.1084/jem.20130497. Epub 2013 Sep 30.

Abstract

Differentiation arrest is a hallmark of acute leukemia. Genomic alterations in B cell differentiation factors such as PAX5, IKZF1, and EBF-1 have been identified in more than half of all cases of childhood B precursor acute lymphoblastic leukemia (ALL). Here, we describe a perturbed epigenetic and transcriptional regulation of ZNF423 in ALL as a novel mechanism interfering with B cell differentiation. Hypomethylation of ZNF423 regulatory sequences and BMP2 signaling result in transactivation of ZNF423α and a novel ZNF423β-isoform encoding a nucleosome remodeling and histone deacetylase complex-interacting domain. Aberrant ZNF423 inhibits the transactivation of EBF-1 target genes and leads to B cell maturation arrest in vivo. Importantly, ZNF423 expression is associated with poor outcome of ETV6-RUNX1-negative B precursor ALL patients. Our work demonstrates that ALL is more than a genetic disease and that epigenetics may uncover novel mechanisms of disease with prognostic implications.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B-Lymphocytes / metabolism
  • B-Lymphocytes / pathology*
  • Bone Morphogenetic Protein 2 / metabolism
  • Cell Differentiation* / genetics
  • Cell Lineage / genetics
  • Core Binding Factor Alpha 2 Subunit / metabolism*
  • DNA Methylation / genetics
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Disease-Free Survival
  • Gene Expression Profiling
  • Gene Expression Regulation, Leukemic
  • Hematopoietic Stem Cells / metabolism
  • Mi-2 Nucleosome Remodeling and Deacetylase Complex / metabolism
  • Mice
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism
  • Oncogene Proteins, Fusion / metabolism*
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma / genetics
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma / pathology*
  • Prognosis
  • Protein Binding / genetics
  • Protein Isoforms / metabolism
  • Protein Structure, Tertiary
  • Proteins
  • Signal Transduction / genetics
  • Smad Proteins / metabolism
  • Trans-Activators / genetics
  • Transcriptional Activation / genetics
  • Up-Regulation / genetics

Substances

  • BMP2 protein, human
  • Bone Morphogenetic Protein 2
  • Core Binding Factor Alpha 2 Subunit
  • DNA-Binding Proteins
  • EBF1 protein, human
  • Neoplasm Proteins
  • Oncogene Proteins, Fusion
  • Protein Isoforms
  • Proteins
  • Smad Proteins
  • TEL-AML1 fusion protein
  • Trans-Activators
  • ornithine decarboxylase antizyme
  • Mi-2 Nucleosome Remodeling and Deacetylase Complex