PHF6 regulates phenotypic plasticity through chromatin organization within lineage-specific genes

Genes Dev. 2017 May 15;31(10):973-989. doi: 10.1101/gad.295857.117. Epub 2017 Jun 12.

Abstract

Developmental and lineage plasticity have been observed in numerous malignancies and have been correlated with tumor progression and drug resistance. However, little is known about the molecular mechanisms that enable such plasticity to occur. Here, we describe the function of the plant homeodomain finger protein 6 (PHF6) in leukemia and define its role in regulating chromatin accessibility to lineage-specific transcription factors. We show that loss of Phf6 in B-cell leukemia results in systematic changes in gene expression via alteration of the chromatin landscape at the transcriptional start sites of B-cell- and T-cell-specific factors. Additionally, Phf6KO cells show significant down-regulation of genes involved in the development and function of normal B cells, show up-regulation of genes involved in T-cell signaling, and give rise to mixed-lineage lymphoma in vivo. Engagement of divergent transcriptional programs results in phenotypic plasticity that leads to altered disease presentation in vivo, tolerance of aberrant oncogenic signaling, and differential sensitivity to frontline and targeted therapies. These findings suggest that active maintenance of a precise chromatin landscape is essential for sustaining proper leukemia cell identity and that loss of a single factor (PHF6) can cause focal changes in chromatin accessibility and nucleosome positioning that render cells susceptible to lineage transition.

Keywords: PHF6; chromatin regulation; leukemia; lineage maintenance; nucleosome positioning; phenotypic plasticity.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Lineage / genetics
  • Chromatin / genetics*
  • Chromatin / metabolism
  • Drug Resistance, Neoplasm / genetics
  • Gene Expression Regulation, Neoplastic*
  • Gene Knockout Techniques
  • Homeodomain Proteins / genetics*
  • Homeodomain Proteins / metabolism*
  • Leukemia, B-Cell / genetics*
  • Leukemia, B-Cell / physiopathology*
  • Lymphoma, Non-Hodgkin / genetics
  • Mice
  • Mice, Inbred C57BL
  • Phenotype
  • Repressor Proteins
  • Signal Transduction / genetics

Substances

  • Chromatin
  • Homeodomain Proteins
  • Phf6 protein, mouse
  • Repressor Proteins