β-Arrestin2 Couples Metabotropic Glutamate Receptor 5 to Neuronal Protein Synthesis and Is a Potential Target to Treat Fragile X

Cell Rep. 2017 Mar 21;18(12):2807-2814. doi: 10.1016/j.celrep.2017.02.075.

Abstract

Synaptic protein synthesis is essential for modification of the brain by experience and is aberrant in several genetically defined disorders, notably fragile X (FX), a heritable cause of autism and intellectual disability. Neural activity directs local protein synthesis via activation of metabotropic glutamate receptor 5 (mGlu5), yet how mGlu5 couples to the intracellular signaling pathways that regulate mRNA translation is poorly understood. Here, we provide evidence that β-arrestin2 mediates mGlu5-stimulated protein synthesis in the hippocampus and show that genetic reduction of β-arrestin2 corrects aberrant synaptic plasticity and cognition in the Fmr1-/y mouse model of FX. Importantly, reducing β-arrestin2 does not induce psychotomimetic activity associated with full mGlu5 inhibitors and does not affect Gq signaling. Thus, in addition to identifying a key requirement for mGlu5-stimulated protein synthesis, these data suggest that β-arrestin2-biased negative modulators of mGlu5 offer significant advantages over first-generation inhibitors for the treatment of FX and related disorders.

Keywords: ERK; autism; biased ligands; fragile X; intellectual disability; long-term depression; mGluR5; metabotropic glutamate receptors; synaptic protein synthesis; β-arrestin2.

Publication types

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

MeSH terms

  • Animals
  • Behavior, Animal
  • Disease Models, Animal
  • Dizocilpine Maleate / pharmacology
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Female
  • Fragile X Mental Retardation Protein / metabolism
  • Fragile X Syndrome / metabolism*
  • Fragile X Syndrome / therapy*
  • GTP-Binding Protein alpha Subunits, Gq-G11
  • Gene Deletion
  • Heterozygote
  • Hippocampus / pathology
  • Hippocampus / physiopathology
  • Locomotion / drug effects
  • Male
  • Mice, Inbred C57BL
  • Molecular Targeted Therapy*
  • Mutation / genetics
  • Neuronal Plasticity
  • Neurons / drug effects
  • Neurons / metabolism*
  • Protein Biosynthesis* / drug effects
  • Receptor, Metabotropic Glutamate 5 / metabolism*
  • Signal Transduction
  • beta-Arrestin 2 / metabolism*

Substances

  • Receptor, Metabotropic Glutamate 5
  • beta-Arrestin 2
  • Fragile X Mental Retardation Protein
  • Dizocilpine Maleate
  • Extracellular Signal-Regulated MAP Kinases
  • GTP-Binding Protein alpha Subunits, Gq-G11