LGI1 downregulation increases neuronal circuit excitability

Epilepsia. 2020 Dec;61(12):2836-2846. doi: 10.1111/epi.16736. Epub 2020 Oct 26.

Abstract

Objective: Leucine-rich glioma-inactivated 1 (LGI1) is a secreted transsynaptic protein that interacts presynaptically with Kv1.1 potassium channels and a disintegrin and metalloprotease (ADAM) protein 23, and postsynaptically influences α-amino-3-hydroxy-5-methylisoxazole-4-propionate receptors through a direct link with the ADAM22 cell adhesion protein. Haploinsufficiency of LGI1 or autoantibodies directed against LGI1 are associated with human epilepsy, generating the hypothesis that a subacute reduction of LGI1 is sufficient to increase network excitability.

Methods: We tested this hypothesis in ex vivo hippocampal slices and in neuronal cultures, by subacutely reducing LGI1 expression with shRNA.

Results: Injection of shRNA-LGI1 in the hippocampus increased dentate granule cell excitability and low-frequency facilitation of mossy fibers to CA3 pyramidal cell neurotransmission. Application of the Kv1 family blocker, α-dendrotoxin, occluded this effect, implicating the involvement of Kv1.1. This subacute reduction of LGI1 was also sufficient to increase neuronal network activity in neuronal primary culture.

Significance: These results indicate that a subacute reduction in LGI1 potentiates neuronal excitability and short-term synaptic plasticity, and increases neuronal network excitability, opening new avenues for the treatment of limbic encephalitis and temporal lobe epilepsies.

Keywords: Kv1.1; LGI1; epilepsy; short-term plasticity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Down-Regulation
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Intracellular Signaling Peptides and Proteins / physiology*
  • Kv1.1 Potassium Channel / metabolism
  • Kv1.1 Potassium Channel / physiology
  • Mice
  • Mice, Knockout
  • Neurons / physiology*
  • Paracrine Communication
  • RNA, Small Interfering
  • Seizures / etiology*
  • Seizures / physiopathology
  • Synapses / metabolism
  • Synapses / physiology

Substances

  • Intracellular Signaling Peptides and Proteins
  • Lgi1 protein, mouse
  • RNA, Small Interfering
  • Kv1.1 Potassium Channel