Phosphatase of regenerating liver-3 is regulated by signal transducer and activator of transcription 3 in acute myeloid leukemia

Exp Hematol. 2014 Dec;42(12):1041-52.e1-2. doi: 10.1016/j.exphem.2014.08.001. Epub 2014 Aug 17.

Abstract

Overexpression of protein-tyrosine phosphatase of regenerating liver 3 (PRL-3) has been identified in about 50% of patients with acute myeloid leukemia (AML). The mechanism of regulation of PRL-3 remains obscure. Signal transducer and activator of transcription 3 (STAT3), a latent transcriptional factor, has also been often found to be activated in AML. We first identified STAT3-consensus-binding sites in the promoter of PRL-3 genes. Then we experimentally validated the direct binding and transcriptional activation. We applied shRNA-mediated knockdown and overexpression approaches in STAT3(-/-) liver cells and leukemic cells to validate the functional regulation of PRL-3 by STAT3. A STAT3 core signature, derived through data mining from publicly available gene expression data, was employed to correlate PRL-3 expression in large AML patient samples. We discovered that STAT3 binds to the -201 to -210 region of PRL-3, which was conserved between human and mouse. Importantly, PRL-3 protein was significantly reduced in mouse STAT3-knockout liver cells compared with STAT3-wild type counterparts, and ectopic expression of STAT3 in these cells led to a pronounced increase in PRL-3 protein. We demonstrated that STAT3 functionally regulated PRL-3, and STAT3 core signature was enriched in AML with high PRL-3 expression. Targeting either STAT3 or PRL-3 reduced leukemic cell viability. Silencing PRL-3 impaired invasiveness and induced leukemic cell differentiation. In conclusion, PRL-3 was transcriptionally regulated by STAT3. The STAT3/PRL-3 regulatory loop contributes to the pathogenesis of AML, and it might represent an attractive therapeutic target for antileukemic therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Binding Sites
  • Cell Differentiation
  • Cell Line, Tumor
  • Conserved Sequence
  • DNA Mutational Analysis
  • DNA, Neoplasm / genetics
  • Gene Dosage
  • Gene Expression Regulation, Leukemic
  • Genes, Reporter
  • Humans
  • Immediate-Early Proteins / biosynthesis
  • Immediate-Early Proteins / genetics
  • Immediate-Early Proteins / physiology*
  • Leukemia, Myeloid, Acute / enzymology*
  • Leukemia, Myeloid, Acute / genetics
  • Liver / metabolism
  • Mice
  • Mutagenesis, Site-Directed
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / physiology*
  • Promoter Regions, Genetic / genetics
  • Protein Tyrosine Phosphatases / biosynthesis
  • Protein Tyrosine Phosphatases / genetics
  • Protein Tyrosine Phosphatases / physiology*
  • RNA Interference
  • RNA, Small Interfering / pharmacology
  • STAT3 Transcription Factor / deficiency
  • STAT3 Transcription Factor / physiology*
  • Signal Transduction
  • Species Specificity
  • Transfection

Substances

  • DNA, Neoplasm
  • Immediate-Early Proteins
  • Neoplasm Proteins
  • Ptp4a3 protein, mouse
  • RNA, Small Interfering
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Stat3 protein, mouse
  • PTP4A3 protein, human
  • Protein Tyrosine Phosphatases