Size distribution of retrovirally marked lineages matches prediction from population measurements of cell cycle behavior

Li Cai, Nancy L. Hayes, Takao Takahashi, Verne S. Caviness, Richard S. Nowakowski

Research output: Contribution to journalArticle

49 Citations (Scopus)

Abstract

Mechanisms that regulate neuron production in the developing mouse neocortex were examined by using a retroviral lineage marking method to determine the sizes of the lineages remaining in the proliferating population of the ventricular zone during the period of neuron production. The distribution of clade sizes obtained experimentally in four different injection-survival paradigms (E11-E13, E11-E14, E11-E15, and E12-E15) from a total of over 500 labeled lineages was compared with that obtained from three models in which the average behavior of the proliferating population [i.e., the proportion of cells remaining in the proliferative population (P) vs. that exiting the proliferative population (Q)] was quantitatively related to lineage size distribution. In model 1, different proportions of asymmetric, symmetric terminal, and symmetric nonterminal cell divisions coexisted during the entire developmental period. In model 2, the developmental period was divided into two epochs: During the first, asymmetric and symmetric nonterminal cell divisions occurred, but, during the second, asymmetric and symmetric terminal cell divisions occurred. In model 3, the shifts in P and Q are accounted for by changes in the proportions of the two types of symmetric cell divisions without the inclusion of any asymmetric cell divisions. The results obtained from the retroviral experiments were well accounted for by model 1 but not by model 2 or 3. These findings demonstrate that: 1) asymmetric and both types of symmetric cell divisions coexist during the entire period of neuronogenesis in the mouse, 2) neuron production is regulated in the proliferative population by the independent decisions of the two daughter cells to reenter S phase, and 3) neurons are produced by both asymmetric and symmetric terminal cell divisions. In addition, the findings mean that cell death and/or tangential movements of cells in the proliferative population occur at only a low rate and that there are no proliferating lineages "reserved" to make particular laminae or cell types.

Original languageEnglish
Pages (from-to)731-744
Number of pages14
JournalJournal of Neuroscience Research
Volume69
Issue number6
DOIs
Publication statusPublished - 2002 Sep 15

Fingerprint

Cell Division
Cell Cycle
Population
Neurons
Asymmetric Cell Division
Neocortex
S Phase
Cell Movement
Cell Death
Injections

Keywords

  • Asymmetric cell divisions
  • Symmetric cell divisions
  • Ventricular zone

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Size distribution of retrovirally marked lineages matches prediction from population measurements of cell cycle behavior. / Cai, Li; Hayes, Nancy L.; Takahashi, Takao; Caviness, Verne S.; Nowakowski, Richard S.

In: Journal of Neuroscience Research, Vol. 69, No. 6, 15.09.2002, p. 731-744.

Research output: Contribution to journalArticle

Cai, Li ; Hayes, Nancy L. ; Takahashi, Takao ; Caviness, Verne S. ; Nowakowski, Richard S. / Size distribution of retrovirally marked lineages matches prediction from population measurements of cell cycle behavior. In: Journal of Neuroscience Research. 2002 ; Vol. 69, No. 6. pp. 731-744.
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