Molecular cascade reveals sequential milestones underlying hippocampal neural stem cell development into an adult state

Cell Rep. 2024 Jun 25;43(6):114339. doi: 10.1016/j.celrep.2024.114339. Epub 2024 Jun 8.

Abstract

Quiescent adult neural stem cells (NSCs) in the mammalian brain arise from proliferating NSCs during development. Beyond acquisition of quiescence, an adult NSC hallmark, little is known about the process, milestones, and mechanisms underlying the transition of developmental NSCs to an adult NSC state. Here, we performed targeted single-cell RNA-seq analysis to reveal the molecular cascade underlying NSC development in the early postnatal mouse dentate gyrus. We identified two sequential steps, first a transition to quiescence followed by further maturation, each of which involved distinct changes in metabolic gene expression. Direct metabolic analysis uncovered distinct milestones, including an autophagy burst before NSC quiescence acquisition and cellular reactive oxygen species level elevation along NSC maturation. Functionally, autophagy is important for the NSC transition to quiescence during early postnatal development. Together, our study reveals a multi-step process with defined milestones underlying establishment of the adult NSC pool in the mammalian brain.

Keywords: CP: Cell biology; CP: Neuroscience; Neural stem cells; adult stem cells; cell state transition; cellular metabolism; dentate gyrus; hippocampus; neural development; quiescence.

MeSH terms

  • Adult Stem Cells / cytology
  • Adult Stem Cells / metabolism
  • Animals
  • Autophagy*
  • Cell Differentiation
  • Cell Proliferation
  • Dentate Gyrus / cytology
  • Dentate Gyrus / growth & development
  • Dentate Gyrus / metabolism
  • Hippocampus* / cytology
  • Hippocampus* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Neural Stem Cells* / cytology
  • Neural Stem Cells* / metabolism
  • Neurogenesis
  • Reactive Oxygen Species / metabolism
  • Single-Cell Analysis

Substances

  • Reactive Oxygen Species