Differences in the mechanical properties of the developing cerebral cortical proliferative zone between mice and ferrets at both the tissue and single-cell levels

Arata Nagasaka, Tomoyasu Shinoda, Takumi Kawaue, Makoto Suzuki, Kazuaki Nagayama, Takeo Matsumoto, Naoto Ueno, Ayano Kawaguchi, Takaki Miyata

Research output: Contribution to journalArticlepeer-review

21 Citations (Scopus)

Abstract

Cell-producing events in developing tissues are mechanically dynamic throughout the cell cycle. In many epithelial systems, cells are apicobasally tall, with nuclei and somata that adopt different apicobasal positions because nuclei and somata move in a cell cycle-dependent manner. This movement is apical during G2 phase and basal during G1 phase, whereas mitosis occurs at the apical surface. These movements are collectively referred to as interkinetic nuclear migration, and such epithelia are called "pseudostratified." The embryonic mammalian cerebral cortical neuroepithelium is a good model for highly pseudostratified epithelia, and we previously found differences between mice and ferrets in both horizontal cellular density (greater in ferrets) and nuclear/somal movements (slower during G2 and faster during G1 in ferrets). These differences suggest that neuroepithelial cells alter their nucleokinetic behavior in response to physical factors that they encounter, which may form the basis for evolutionary transitions toward more abundant brain-cell production from mice to ferrets and primates. To address how mouse and ferret neuroepithelia may differ physically in a quantitative manner, we used atomic force microscopy to determine that the vertical stiffness of their apical surface is greater in ferrets (Young's modulus = 1700 Pa) than in mice (1400 Pa). We systematically analyzed factors underlying the apical-surface stiffness through experiments to pharmacologically inhibit actomyosin or microtubules and to examine recoiling behaviors of the apical surface upon laser ablation and also through electron microscopy to observe adherens junction. We found that although both actomyosin and microtubules are partly responsible for the apical-surface stiffness, the mouse<ferret relationship in the apical-surface stiffness was maintained even in the presence of inhibitors. We also found that the stiffness of single, dissociated neuroepithelial cells is actually greater in mice (720 Pa) than in ferrets (450 Pa). Adherens junction was ultrastructurally comparable between mice and ferrets. These results show that the horizontally denser packing of neuroepithelial cell processes is a major contributor to the increased tissue-level apical stiffness in ferrets, and suggest that tissue-level mechanical properties may be achieved by balancing cellular densification and the physical properties of single cells.

Original languageEnglish
Article number139
JournalFrontiers in Cell and Developmental Biology
Volume4
Issue numberNOV
DOIs
Publication statusPublished - Nov 25 2016
Externally publishedYes

Keywords

  • Actomyosin
  • Apical surface
  • Atomic force microscopy
  • Cell density
  • Elasticity
  • Interkinetic nuclear migration
  • Neural progenitor cell
  • Neuroepithelium

ASJC Scopus subject areas

  • Developmental Biology
  • Cell Biology

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