GSK3β Inhibition Restores Impaired Neurogenesis in Preterm Neonates With Intraventricular Hemorrhage

Cereb Cortex. 2019 Jul 22;29(8):3482-3495. doi: 10.1093/cercor/bhy217.

Abstract

Intraventricular hemorrhage (IVH) is a common complication of prematurity in infants born at 23-28 weeks of gestation. Survivors exhibit impaired growth of the cerebral cortex and neurodevelopmental sequeale, but the underlying mechanism(s) are obscure. Previously, we have shown that neocortical neurogenesis continues until at least 28 gestational weeks. This renders the prematurely born infants vulnerable to impaired neurogenesis. Here, we hypothesized that neurogenesis is impaired by IVH, and that signaling through GSK3β, a critical intracellular kinase regulated by Wnt and other pathways, mediates this effect. These hypotheses were tested observationally in autopsy specimens from premature infants, and experimentally in a premature rabbit IVH model. Significantly, in premature infants with IVH, the number of neurogenic cortical progenitor cells was reduced compared with infants without IVH, indicating acutely decreased neurogenesis. This finding was corroborated in the rabbit IVH model, which further demonstrated reduction of upper layer cortical neurons after longer survival. Both the acute reduction of neurogenic progenitors, and the subsequent decrease of upper layer neurons, were rescued by treatment with AR-A014418, a specific inhibitor of GSK3β. Together, these results indicate that IVH impairs late stages of cortical neurogenesis, and suggest that treatment with GSK3β inhibitors may enhance neurodevelopment in premature infants with IVH.

Keywords: GSK3β; Pax6; Tbr2; intermediate progenitors; intraventricular hemorrhage; neurogenesis.

MeSH terms

  • Animals
  • Apoptosis / drug effects*
  • Blotting, Western
  • Case-Control Studies
  • Cell Count
  • Cell Proliferation
  • Cerebral Cortex
  • Cerebral Intraventricular Hemorrhage / metabolism*
  • Cerebral Intraventricular Hemorrhage / pathology
  • Disease Models, Animal
  • Ependymoglial Cells / drug effects
  • Ependymoglial Cells / metabolism
  • Glycogen Synthase Kinase 3 beta / antagonists & inhibitors*
  • Humans
  • Immunohistochemistry
  • Infant, Extremely Premature
  • Infant, Newborn
  • Ki-67 Antigen / metabolism
  • Lateral Ventricles
  • Neural Stem Cells / drug effects*
  • Neural Stem Cells / metabolism
  • Neural Stem Cells / pathology
  • Neurogenesis / drug effects*
  • PAX6 Transcription Factor / metabolism
  • Phosphorylation
  • Pyramidal Cells / drug effects
  • Pyramidal Cells / metabolism
  • Pyramidal Cells / pathology
  • Rabbits
  • Real-Time Polymerase Chain Reaction
  • Retinoblastoma Protein / metabolism
  • SOXB1 Transcription Factors / metabolism
  • T-Box Domain Proteins / metabolism
  • Thiazoles / pharmacology*
  • Urea / analogs & derivatives*
  • Urea / pharmacology
  • White Matter

Substances

  • EOMES protein, human
  • Ki-67 Antigen
  • MKI67 protein, human
  • PAX6 Transcription Factor
  • Retinoblastoma Protein
  • SOX2 protein, human
  • SOXB1 Transcription Factors
  • T-Box Domain Proteins
  • Thiazoles
  • N-(4-methoxybenzyl)-N'-(5-nitro-1,3-thiazol-2-yl)urea
  • Urea
  • Glycogen Synthase Kinase 3 beta