FLNA regulates neuronal maturation by modulating RAC1-Cofilin activity in the developing cortex

Neurobiol Dis. 2024 Aug:198:106558. doi: 10.1016/j.nbd.2024.106558. Epub 2024 Jun 7.

Abstract

Periventricular nodular heterotopia (PNH), the most common brain malformation diagnosed in adulthood, is characterized by the presence of neuronal nodules along the ventricular walls. PNH is mainly associated with mutations in the FLNA gene - encoding an actin-binding protein - and patients often develop epilepsy. However, the molecular mechanisms underlying the neuronal failure still remain elusive. It has been hypothesized that dysfunctional cortical circuitry, rather than ectopic neurons, may explain the clinical manifestations. To address this issue, we depleted FLNA from cortical pyramidal neurons of a conditional Flnaflox/flox mice by timed in utero electroporation of Cre recombinase. We found that FLNA regulates dendritogenesis and spinogenesis thus promoting an appropriate excitatory/inhibitory inputs balance. We demonstrated that FLNA modulates RAC1 and cofilin activity through its interaction with the Rho-GTPase Activating Protein 24 (ARHGAP24). Collectively, we disclose an uncharacterized role of FLNA and provide strong support for neural circuit dysfunction being a consequence of FLNA mutations.

Keywords: Animal model; Brain development; Dendritogenesis -neurodevelopmental disorders; Neuronal maturation.

MeSH terms

  • Actin Depolymerizing Factors / metabolism
  • Animals
  • Cerebral Cortex* / metabolism
  • Filamins* / genetics
  • Filamins* / metabolism
  • GTPase-Activating Proteins / genetics
  • GTPase-Activating Proteins / metabolism
  • Mice
  • Mice, Transgenic
  • Neurogenesis / physiology
  • Neurons / metabolism
  • Neuropeptides / genetics
  • Neuropeptides / metabolism
  • Periventricular Nodular Heterotopia / genetics
  • Periventricular Nodular Heterotopia / metabolism
  • Periventricular Nodular Heterotopia / pathology
  • Pyramidal Cells / metabolism
  • rac1 GTP-Binding Protein* / genetics
  • rac1 GTP-Binding Protein* / metabolism

Substances

  • Actin Depolymerizing Factors
  • Filamins
  • FlnA protein, mouse
  • GTPase-Activating Proteins
  • Neuropeptides
  • rac1 GTP-Binding Protein
  • Rac1 protein, mouse
  • Cfl1 protein, mouse