Mapping differentiation kinetics in the mouse retina reveals an extensive period of cell cycle protein expression in post-mitotic newborn neurons

Dev Dyn. 2012 Oct;241(10):1525-44. doi: 10.1002/dvdy.23840. Epub 2012 Aug 13.

Abstract

Background: Knowledge of gene expression kinetics around neuronal cell birth is required to dissect mechanisms underlying progenitor fate. Here, we timed cell cycle and neuronal protein silencing/induction during cell birth in the developing murine retina.

Results: The pan-cell cycle markers Pcna and Mcm6 were present in the post-mitotic ganglion cell layer. Although confined to the neuroblastic layer (NBL), 6-7% of Ki67(+) cells lacked six progenitor/cell cycle markers, and expressed neuronal markers. To define protein extinction/induction timing, we defined G2/M length throughout retinogenesis, which was typically 1-2 h, but <10% cells took double this time. BrdU-chase analyses revealed that at E12.5, Tubb3 (Tuj1) appeared at M-phase, followed by Calb2 and Dcx at ~2 h, Elavl2/3/4 at ~4 h, and Map2 at ~6 h after cell birth, and these times extended with embryonic age. Strikingly, Ki67 was not extinguished until up to a day after cell cycle exit, coinciding with exit from the NBL and induction of late markers such as Map1b/Uchl1/Rbfox3.

Conclusions: A minor population of progenitors transits slowly through G2/M and, most importantly, some cell cycle proteins are retained for an unexpectedly long period in post-mitotic neurons. The high-resolution map of cell birth kinetics reported here provides a framework to better define mechanisms that regulate neurogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn / physiology*
  • Bromodeoxyuridine
  • Cell Cycle Proteins / metabolism*
  • Cell Differentiation / physiology*
  • Doublecortin Protein
  • G2 Phase Cell Cycle Checkpoints / physiology
  • Gene Expression Regulation, Developmental / physiology*
  • Image Processing, Computer-Assisted
  • Ki-67 Antigen / metabolism
  • Mice
  • Microscopy, Confocal
  • Minichromosome Maintenance Complex Component 6
  • Neurons / metabolism*
  • Neurons / physiology
  • Proliferating Cell Nuclear Antigen / metabolism
  • Retina / cytology*
  • Retina / growth & development
  • Time Factors

Substances

  • Cell Cycle Proteins
  • Dcx protein, mouse
  • Doublecortin Protein
  • Ki-67 Antigen
  • Proliferating Cell Nuclear Antigen
  • Mcm6 protein, mouse
  • Minichromosome Maintenance Complex Component 6
  • Bromodeoxyuridine