Raptor-Mediated Proteasomal Degradation of Deamidated 4E-BP2 Regulates Postnatal Neuronal Translation and NF-κB Activity

Cell Rep. 2019 Dec 10;29(11):3620-3635.e7. doi: 10.1016/j.celrep.2019.11.023.

Abstract

The translation initiation repressor 4E-BP2 is deamidated in the brain on asparagines N99/N102 during early postnatal brain development. This post-translational modification enhances 4E-BP2 association with Raptor, a central component of mTORC1 and alters the kinetics of excitatory synaptic transmission. We show that 4E-BP2 deamidation is neuron specific, occurs in the human brain, and changes 4E-BP2 subcellular localization, but not its disordered structure state. We demonstrate that deamidated 4E-BP2 is ubiquitinated more and degrades faster than the unmodified protein. We find that enhanced deamidated 4E-BP2 degradation is dependent on Raptor binding, concomitant with increased association with a Raptor-CUL4B E3 ubiquitin ligase complex. Deamidated 4E-BP2 stability is promoted by inhibiting mTORC1 or glutamate receptors. We further demonstrate that deamidated 4E-BP2 regulates the translation of a distinct pool of mRNAs linked to cerebral development, mitochondria, and NF-κB activity, and thus may be crucial for postnatal brain development in neurodevelopmental disorders, such as ASD.

Keywords: 4E-BP2; CUL4B; NF-κB; Raptor; asparagine deamidation; mTORC1; postnatal brain; proteasome; translational control.

MeSH terms

  • Animals
  • Brain / cytology
  • Brain / metabolism
  • Cells, Cultured
  • Cullin Proteins / metabolism
  • Eukaryotic Initiation Factors / metabolism*
  • Female
  • HEK293 Cells
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • NF-kappa B / metabolism*
  • Neurons / metabolism*
  • Proteasome Endopeptidase Complex / metabolism*
  • Protein Binding
  • Proteolysis
  • Regulatory-Associated Protein of mTOR / metabolism*

Substances

  • Cul4B protein, mouse
  • Cullin Proteins
  • Eif4ebp2 protein, mouse
  • Eukaryotic Initiation Factors
  • NF-kappa B
  • Regulatory-Associated Protein of mTOR
  • Rptor protein, mouse
  • Proteasome Endopeptidase Complex