NPRL2 Inhibition of mTORC1 Controls Sodium Channel Expression and Brain Amino Acid Homeostasis

eNeuro. 2022 Mar 3;9(2):ENEURO.0317-21.2022. doi: 10.1523/ENEURO.0317-21.2022. Print 2022 Mar-Apr.

Abstract

Genetic mutations in nitrogen permease regulator-like 2 (NPRL2) are associated with a wide spectrum of familial focal epilepsies, autism, and sudden unexpected death of epileptics (SUDEP), but the mechanisms by which NPRL2 contributes to these effects are not well known. NPRL2 is a requisite subunit of the GAP activity toward Rags 1 (GATOR1) complex, which functions as a negative regulator of mammalian target of rapamycin complex 1 (mTORC1) kinase when intracellular amino acids are low. Here, we show that loss of NPRL2 expression in mouse excitatory glutamatergic neurons causes seizures before death, consistent with SUDEP in humans with epilepsy. Additionally, the absence of NPRL2 expression increases mTORC1-dependent signal transduction and significantly alters amino acid homeostasis in the brain. Loss of NPRL2 reduces dendritic branching and increases the strength of electrically stimulated action potentials (APs) in neurons. The increased AP strength is consistent with elevated expression of epilepsy-linked, voltage-gated sodium channels in the NPRL2-deficient brain. Targeted deletion of NPRL2 in primary neurons increases the expression of sodium channel Scn1A, whereas treatment with the pharmacological mTORC1 inhibitor called rapamycin prevents Scn1A upregulation. These studies demonstrate a novel role of NPRL2 and mTORC1 signaling in the regulation of sodium channels, which can contribute to seizures and early lethality.

Keywords: GATOR1; NPRL2; epilepsy; mTORC1; neurometabolism; sodium channels.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids
  • Animals
  • Brain / metabolism
  • Homeostasis
  • Mammals / metabolism
  • Mechanistic Target of Rapamycin Complex 1 / metabolism
  • Membrane Transport Proteins* / metabolism
  • Mice
  • NAV1.1 Voltage-Gated Sodium Channel / metabolism
  • Nitrogen / metabolism
  • Sodium Channels / metabolism
  • Tumor Suppressor Proteins* / chemistry
  • Tumor Suppressor Proteins* / genetics
  • Tumor Suppressor Proteins* / metabolism

Substances

  • Amino Acids
  • Membrane Transport Proteins
  • NAV1.1 Voltage-Gated Sodium Channel
  • Scn1a protein, mouse
  • Sodium Channels
  • Tumor Suppressor Proteins
  • Mechanistic Target of Rapamycin Complex 1
  • Nitrogen