Molecular determinants and signaling effects of PKA RIα phase separation

Mol Cell. 2024 Apr 18;84(8):1570-1584.e7. doi: 10.1016/j.molcel.2024.03.002. Epub 2024 Mar 26.

Abstract

Spatiotemporal regulation of intracellular signaling molecules, such as the 3',5'-cyclic adenosine monophosphate (cAMP)-dependent protein kinase (PKA), ensures proper cellular function. Liquid-liquid phase separation (LLPS) of the ubiquitous PKA regulatory subunit RIα promotes cAMP compartmentation and signaling specificity. However, the molecular determinants of RIα LLPS remain unclear. Here, we reveal that two separate dimerization interfaces, combined with the cAMP-induced unleashing of the PKA catalytic subunit (PKA-C) from the pseudosubstrate inhibitory sequence, drive RIα condensate formation in the cytosol of mammalian cells, which is antagonized by docking to A-kinase anchoring proteins. Strikingly, we find that the RIα pseudosubstrate region is critically involved in forming a non-canonical R:C complex, which recruits active PKA-C to RIα condensates to maintain low basal PKA activity in the cytosol. Our results suggest that RIα LLPS not only facilitates cAMP compartmentation but also spatially restrains active PKA-C, thus highlighting the functional versatility of biomolecular condensates in driving signaling specificity.

Keywords: biomolecular condensates; intrinsically disordered region; protein kinase; signaling compartmentation.

MeSH terms

  • Animals
  • Cyclic AMP / metabolism
  • Cyclic AMP-Dependent Protein Kinase RIalpha Subunit* / chemistry
  • Cyclic AMP-Dependent Protein Kinase RIalpha Subunit* / genetics
  • Cyclic AMP-Dependent Protein Kinase RIalpha Subunit* / metabolism
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Mammals / metabolism
  • Phase Separation*
  • Signal Transduction

Substances

  • Cyclic AMP-Dependent Protein Kinase RIalpha Subunit
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases