C6 pyridinium ceramide influences alternative pre-mRNA splicing by inhibiting protein phosphatase-1

Nucleic Acids Res. 2012 May;40(9):4025-39. doi: 10.1093/nar/gkr1289. Epub 2011 Dec 30.

Abstract

Alternative pre-mRNA processing is a central element of eukaryotic gene regulation. The cell frequently alters the use of alternative exons in response to physiological stimuli. Ceramides are lipid-signaling molecules composed of sphingosine and a fatty acid. Previously, water-insoluble ceramides were shown to change alternative splicing and decrease SR-protein phosphorylation by activating protein phosphatase-1 (PP1). To gain further mechanistical insight into ceramide-mediated alternative splicing, we analyzed the effect of C6 pyridinium ceramide (PyrCer) on alternative splice site selection. PyrCer is a water-soluble ceramide analog that is under investigation as a cancer drug. We found that PyrCer binds to the PP1 catalytic subunit and inhibits the dephosphorylation of several splicing regulatory proteins containing the evolutionarily conserved RVxF PP1-binding motif (including PSF/SFPQ, Tra2-beta1 and SF2/ASF). In contrast to natural ceramides, PyrCer promotes phosphorylation of splicing factors. Exons that are regulated by PyrCer have in common suboptimal splice sites, are unusually short and share two 4-nt motifs, GAAR and CAAG. They are dependent on PSF/SFPQ, whose phosphorylation is regulated by PyrCer. Our results indicate that lipids can influence pre-mRNA processing by regulating the phosphorylation status of specific regulatory factors, which is mediated by protein phosphatase activity.

Publication types

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

MeSH terms

  • Alternative Splicing / drug effects*
  • Binding Sites
  • Ceramides / pharmacology*
  • Enzyme Inhibitors / pharmacology*
  • Exons
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Phosphorylation / drug effects
  • Protein Phosphatase 1 / antagonists & inhibitors*
  • Pyridinium Compounds / pharmacology*
  • RNA Precursors / metabolism*
  • RNA, Messenger / metabolism*
  • RNA-Binding Proteins / metabolism

Substances

  • 2-N-(6'-(1''-pyridinium)hexanoyl)sphingosine
  • Ceramides
  • Enzyme Inhibitors
  • Pyridinium Compounds
  • RNA Precursors
  • RNA, Messenger
  • RNA-Binding Proteins
  • Protein Phosphatase 1