Regulation of CD44E by DARPP-32-dependent activation of SRp20 splicing factor in gastric tumorigenesis

Oncogene. 2016 Apr 7;35(14):1847-56. doi: 10.1038/onc.2015.250. Epub 2015 Jun 29.

Abstract

CD44E is a frequently overexpressed variant of CD44 in gastric cancer. Mechanisms that regulate CD44 splicing and expression in gastric cancer remain unknown. Herein, we investigated the role of DARPP-32 (dopamine and cyclic adenosine monophosphate-regulated phosphoprotein, Mr 32000) in promoting tumor growth through regulation of CD44 splicing. Using western blot and quantitative real-time PCR analysis, our results indicated that knockdown of endogenous DARPP-32 markedly reduces the expression of CD44 V8-V10 (CD44E). Using a quantitative splicing luciferase reporter system, we detected a significant increase in the reporter activity following DARPP-32 overexpression (P<0.001). Conversely, knocking down endogenous DARPP-32 significantly attenuated the splicing activity (P<0.001). Further experiments showed that DARPP-32 regulates the expression of SRp20 splicing factor and co-exists with it in the same protein complex. Inhibition of alternative splicing with digitoxin followed by immunoprecipitation and immunoblotting indicated that DARPP-32 has an important role in regulating SRp20 protein stability. The knockdown of endogenous DARPP-32 confirmed that DARPP-32 regulates the SRp20-dependent CD44E splicing. Using tumor xenograft mouse model, knocking down endogenous DARPP-32 markedly reduced SRp20 and CD44E protein levels with a decreased tumor growth. The reconstitution of SRp20 expression in these cells rescued tumor growth. In addition, we also demonstrated frequent co-overexpression and positive correlation of DARPP-32, SRp20 and CD44E expression levels in human gastric primary tumors. Our novel findings establish for the first time the role of DARPP-32 in regulating splicing factors in gastric cancer cells. The DARPP-32-SRp20 axis has a key role in regulating the CD44E splice variant that promotes gastric tumorigenesis.

Publication types

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

MeSH terms

  • Alternative Splicing / genetics
  • Animals
  • Carcinogenesis / genetics*
  • Cell Line, Tumor
  • Cell Proliferation
  • Dopamine and cAMP-Regulated Phosphoprotein 32 / genetics*
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Hyaluronan Receptors / biosynthesis
  • Hyaluronan Receptors / genetics*
  • Mice
  • RNA-Binding Proteins / biosynthesis
  • RNA-Binding Proteins / genetics*
  • Serine-Arginine Splicing Factors
  • Signal Transduction / genetics
  • Stomach Neoplasms / genetics*
  • Stomach Neoplasms / pathology
  • Xenograft Model Antitumor Assays

Substances

  • CD44 protein, human
  • Dopamine and cAMP-Regulated Phosphoprotein 32
  • Hyaluronan Receptors
  • PPP1R1B protein, human
  • RNA-Binding Proteins
  • SRSF3 protein, human
  • Serine-Arginine Splicing Factors