Ebf1 or Pax5 haploinsufficiency synergizes with STAT5 activation to initiate acute lymphoblastic leukemia

J Exp Med. 2011 Jun 6;208(6):1135-49. doi: 10.1084/jem.20101947. Epub 2011 May 23.

Abstract

As STAT5 is critical for the differentiation, proliferation, and survival of progenitor B cells, this transcription factor may play a role in acute lymphoblastic leukemia (ALL). Here, we show increased expression of activated signal transducer and activator of transcription 5 (STAT5), which is correlated with poor prognosis, in ALL patient cells. Mutations in EBF1 and PAX5, genes critical for B cell development have also been identified in human ALL. To determine whether mutations in Ebf1 or Pax5 synergize with STAT5 activation to induce ALL, we crossed mice expressing a constitutively active form of STAT5 (Stat5b-CA) with mice heterozygous for Ebf1 or Pax5. Haploinsufficiency of either Pax5 or Ebf1 synergized with Stat5b-CA to rapidly induce ALL in 100% of the mice. The leukemic cells displayed reduced expression of both Pax5 and Ebf1, but this had little effect on most EBF1 or PAX5 target genes. Only a subset of target genes was deregulated; this subset included a large percentage of potential tumor suppressor genes and oncogenes. Further, most of these genes appear to be jointly regulated by both EBF1 and PAX5. Our findings suggest a model whereby small perturbations in a self-reinforcing network of transcription factors critical for B cell development, specifically PAX5 and EBF1, cooperate with STAT5 activation to initiate ALL.

Publication types

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

MeSH terms

  • Animals
  • B-Lymphocytes / cytology
  • Cell Proliferation
  • Gene Expression Regulation, Leukemic*
  • Heterozygote
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mutation*
  • Oligonucleotide Array Sequence Analysis
  • PAX5 Transcription Factor / genetics*
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / genetics
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / metabolism
  • Receptors, Interleukin-7 / metabolism
  • STAT5 Transcription Factor / genetics*
  • STAT5 Transcription Factor / metabolism
  • Trans-Activators / genetics*
  • Treatment Outcome
  • VDJ Recombinases / metabolism

Substances

  • EBF1 protein, human
  • Ebf1 protein, mouse
  • PAX5 Transcription Factor
  • PAX5 protein, human
  • Pax5 protein, mouse
  • Receptors, Interleukin-7
  • STAT5 Transcription Factor
  • Trans-Activators
  • interleukin-7 receptor, alpha chain
  • VDJ Recombinases