FUS-DDIT3 prevents the development of adipocytic precursors in liposarcoma by repressing PPARgamma and C/EBPalpha and activating eIF4E

PLoS One. 2008 Jul 2;3(7):e2569. doi: 10.1371/journal.pone.0002569.

Abstract

Background: FUS-DDIT3 is a chimeric protein generated by the most common chromosomal translocation t(12;16)(q13;p11) linked to liposarcomas, which are characterized by the accumulation of early adipocytic precursors. Current studies indicate that FUS-DDIT3- liposarcoma develops from uncommitted progenitors. However, the precise mechanism whereby FUS-DDIT3 contributes to the differentiation arrest remains to be elucidated.

Methodology/principal findings: Here we have characterized the adipocyte regulatory protein network in liposarcomas of FUS-DITT3 transgenic mice and showed that PPARgamma2 and C/EBPalpha expression was altered. Consistent with in vivo data, FUS-DDIT3 MEFs and human liposarcoma cell lines showed a similar downregulation of both PPARgamma2 and C/EBPalpha expression. Complementation studies with PPARgamma but not C/EBPalpha rescued the differentiation block in committed adipocytic precursors expressing FUS-DDIT3. Our results further show that FUS-DDIT3 interferes with the control of initiation of translation by upregulation of the eukaryotic translation initiation factors eIF2 and eIF4E both in FUS-DDIT3 mice and human liposarcomas cell lines, explaining the shift towards the truncated p30 isoform of C/EBPalpha in liposarcomas. Suppression of the FUS-DDIT3 transgene did rescue this adipocyte differentiation block. Moreover, eIF4E was also strongly upregulated in normal adipose tissue of FUS-DDIT3 transgenic mice, suggesting that overexpression of eIF4E may be a primary event in the initiation of liposarcomas. Reporter assays showed FUS-DDIT3 is involved in the upregulation of eIF4E in liposarcomas and that both domains of the fusion protein are required for affecting eIF4E expression.

Conclusions/significance: Taken together, this study provides evidence of the molecular mechanisms involve in the disruption of normal adipocyte differentiation program in liposarcoma harbouring the chimeric gene FUS-DDIT3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipocytes / cytology*
  • Animals
  • CCAAT-Enhancer-Binding Protein-alpha / antagonists & inhibitors*
  • Cell Line
  • Eukaryotic Initiation Factor-4E / metabolism*
  • Humans
  • Liposarcoma / metabolism*
  • Liposarcoma / pathology
  • Mice
  • Mice, Transgenic
  • Mutant Chimeric Proteins / genetics
  • Mutant Chimeric Proteins / physiology*
  • Oncogene Proteins, Fusion / genetics
  • Oncogene Proteins, Fusion / physiology*
  • PPAR gamma / antagonists & inhibitors*
  • Stem Cells / metabolism
  • Up-Regulation

Substances

  • CCAAT-Enhancer-Binding Protein-alpha
  • Eukaryotic Initiation Factor-4E
  • FUS-DDIT3 fusion protein, human
  • Mutant Chimeric Proteins
  • Oncogene Proteins, Fusion
  • PPAR gamma