The Ras-like GTPase Rem2 is a potent inhibitor of calcium/calmodulin-dependent kinase II activity

J Biol Chem. 2018 Sep 21;293(38):14798-14811. doi: 10.1074/jbc.RA118.003560. Epub 2018 Aug 2.

Abstract

Ca2+/calmodulin-dependent protein kinase II (CaMKII) is a well-characterized, abundant protein kinase that regulates a diverse set of functions in a tissue-specific manner. For example, in heart muscle, CaMKII regulates Ca2+ homeostasis, whereas in neurons, CaMKII regulates activity-dependent dendritic remodeling and long-term potentiation (LTP), a neurobiological correlate of learning and memory. Previously, we identified the GTPase Rem2 as a critical regulator of dendrite branching and homeostatic plasticity in the vertebrate nervous system. Here, we report that Rem2 directly interacts with CaMKII and potently inhibits the activity of the intact holoenzyme, a previously unknown Rem2 function. Our results suggest that Rem2 inhibition involves interaction with both the CaMKII hub domain and substrate recognition domain. Moreover, we found that Rem2-mediated inhibition of CaMKII regulates dendritic branching in cultured hippocampal neurons. Lastly, we report that substitution of two key amino acid residues in the Rem2 N terminus (Arg-79 and Arg-80) completely abolishes its ability to inhibit CaMKII. We propose that our biochemical findings will enable further studies unraveling the functional significance of Rem2 inhibition of CaMKII in cells.

Keywords: Ca2+/calmodulin-dependent protein kinase II (CaMKII); GTPase; RGK family; Rem2; autophosphorylation; calcium; inhibitor; phosphorylation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Calcium / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / antagonists & inhibitors*
  • Cells, Cultured
  • HEK293 Cells
  • Hippocampus / cytology
  • Hippocampus / enzymology
  • Hippocampus / metabolism
  • Homeostasis
  • Humans
  • Learning
  • Long-Term Potentiation
  • Memory
  • Mice
  • Monomeric GTP-Binding Proteins / chemistry
  • Monomeric GTP-Binding Proteins / physiology*
  • Neuronal Plasticity
  • Neurons / metabolism
  • Phosphorylation
  • Substrate Specificity

Substances

  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Monomeric GTP-Binding Proteins
  • REM2 protein, human
  • Rem2 protein, mouse
  • Calcium