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Interkinetic nuclear migration generates and opposes ventricular-zone crowding: insight into tissue mechanics.

Miyata T, Okamoto M, Shinoda T, Kawaguchi A - Front Cell Neurosci (2015)

Bottom Line: This review will summarize and discuss several topics: the nature of the INM exhibited by neural progenitor cells, the mechanical difficulties associated with INM in the developing cerebral cortex, the community-level mechanisms underlying collective and efficient INM, the impact on overall brain formation when NE/VZ is overcrowded due to loss of INM, and whether and how neural progenitor INM varies among mammalian species.These discussions will be based on recent findings obtained in live, three-dimensional specimens using quantitative and mechanical approaches.A consideration of the physical aspects in the NE/VZ and the mechanical difficulties associated with high-degree pseudostratification (PS) is important for achieving a better understanding of neocortical development and evolution.

View Article: PubMed Central - PubMed

Affiliation: Anatomy and Cell Biology, Nagoya University Graduate School of Medicine Nagoya, Aichi, Japan.

ABSTRACT
The neuroepithelium (NE) or ventricular zone (VZ), from which multiple types of brain cells arise, is pseudostratified. In the NE/VZ, neural progenitor cells are elongated along the apicobasal axis, and their nuclei assume different apicobasal positions. These nuclei move in a cell cycle-dependent manner, i.e., apicalward during G2 phase and basalward during G1 phase, a process called interkinetic nuclear migration (INM). This review will summarize and discuss several topics: the nature of the INM exhibited by neural progenitor cells, the mechanical difficulties associated with INM in the developing cerebral cortex, the community-level mechanisms underlying collective and efficient INM, the impact on overall brain formation when NE/VZ is overcrowded due to loss of INM, and whether and how neural progenitor INM varies among mammalian species. These discussions will be based on recent findings obtained in live, three-dimensional specimens using quantitative and mechanical approaches. Experiments in which overcrowding was induced in mouse neocortical NE/VZ, as well as comparisons of neocortical INM between mice and ferrets, have revealed that the behavior of NE/VZ cells can be affected by cellular densification. A consideration of the physical aspects in the NE/VZ and the mechanical difficulties associated with high-degree pseudostratification (PS) is important for achieving a better understanding of neocortical development and evolution.

No MeSH data available.


Comparison between a simple cuboidal epithelium (A) and two columnar epithelia differing in the degree of pseudostratification (B, C). Given that there is a 1:5 ratio between the length of S-phase and the total length of the cell cycle length, and that there is no synchronization between neighboring cells, the number of mitoses at the unit of apical area increases as PS is accelerated, indicating that PS is a means to make epithelia as productive as possible at the apical surface.
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Figure 2: Comparison between a simple cuboidal epithelium (A) and two columnar epithelia differing in the degree of pseudostratification (B, C). Given that there is a 1:5 ratio between the length of S-phase and the total length of the cell cycle length, and that there is no synchronization between neighboring cells, the number of mitoses at the unit of apical area increases as PS is accelerated, indicating that PS is a means to make epithelia as productive as possible at the apical surface.

Mentions: What is the biological significance of high-degree INM-mediated PS of the type observed in the neocortical NE/VZ? In Figure 2, a simple cuboidal epithelium and two differently pseudostratified columnar (two-nuclei–and four-nuclei–deep) epithelia are compared. In the simple cuboidal epithelium, the length of each side of a cell is a. In the pseudostratified epithelia, the longer side of each apical endfoot remains a, whereas the other side of the apex shortens and the apicobasal length of each cell increases. The comparison reveals that increasing the degree of PS along the apicobasal axis may horizontally densify neural progenitors (i.e., increase the number of progenitors per unit of subapical volume and increase the number of mitoses per unit [5a2] of apical surface area). Therefore, high-degree PS allows an epithelial system to increase its productivity at the apical surface (Smart, 1972; Fish et al., 2008; Miyata, 2008).


Interkinetic nuclear migration generates and opposes ventricular-zone crowding: insight into tissue mechanics.

Miyata T, Okamoto M, Shinoda T, Kawaguchi A - Front Cell Neurosci (2015)

Comparison between a simple cuboidal epithelium (A) and two columnar epithelia differing in the degree of pseudostratification (B, C). Given that there is a 1:5 ratio between the length of S-phase and the total length of the cell cycle length, and that there is no synchronization between neighboring cells, the number of mitoses at the unit of apical area increases as PS is accelerated, indicating that PS is a means to make epithelia as productive as possible at the apical surface.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4309187&req=5

Figure 2: Comparison between a simple cuboidal epithelium (A) and two columnar epithelia differing in the degree of pseudostratification (B, C). Given that there is a 1:5 ratio between the length of S-phase and the total length of the cell cycle length, and that there is no synchronization between neighboring cells, the number of mitoses at the unit of apical area increases as PS is accelerated, indicating that PS is a means to make epithelia as productive as possible at the apical surface.
Mentions: What is the biological significance of high-degree INM-mediated PS of the type observed in the neocortical NE/VZ? In Figure 2, a simple cuboidal epithelium and two differently pseudostratified columnar (two-nuclei–and four-nuclei–deep) epithelia are compared. In the simple cuboidal epithelium, the length of each side of a cell is a. In the pseudostratified epithelia, the longer side of each apical endfoot remains a, whereas the other side of the apex shortens and the apicobasal length of each cell increases. The comparison reveals that increasing the degree of PS along the apicobasal axis may horizontally densify neural progenitors (i.e., increase the number of progenitors per unit of subapical volume and increase the number of mitoses per unit [5a2] of apical surface area). Therefore, high-degree PS allows an epithelial system to increase its productivity at the apical surface (Smart, 1972; Fish et al., 2008; Miyata, 2008).

Bottom Line: This review will summarize and discuss several topics: the nature of the INM exhibited by neural progenitor cells, the mechanical difficulties associated with INM in the developing cerebral cortex, the community-level mechanisms underlying collective and efficient INM, the impact on overall brain formation when NE/VZ is overcrowded due to loss of INM, and whether and how neural progenitor INM varies among mammalian species.These discussions will be based on recent findings obtained in live, three-dimensional specimens using quantitative and mechanical approaches.A consideration of the physical aspects in the NE/VZ and the mechanical difficulties associated with high-degree pseudostratification (PS) is important for achieving a better understanding of neocortical development and evolution.

View Article: PubMed Central - PubMed

Affiliation: Anatomy and Cell Biology, Nagoya University Graduate School of Medicine Nagoya, Aichi, Japan.

ABSTRACT
The neuroepithelium (NE) or ventricular zone (VZ), from which multiple types of brain cells arise, is pseudostratified. In the NE/VZ, neural progenitor cells are elongated along the apicobasal axis, and their nuclei assume different apicobasal positions. These nuclei move in a cell cycle-dependent manner, i.e., apicalward during G2 phase and basalward during G1 phase, a process called interkinetic nuclear migration (INM). This review will summarize and discuss several topics: the nature of the INM exhibited by neural progenitor cells, the mechanical difficulties associated with INM in the developing cerebral cortex, the community-level mechanisms underlying collective and efficient INM, the impact on overall brain formation when NE/VZ is overcrowded due to loss of INM, and whether and how neural progenitor INM varies among mammalian species. These discussions will be based on recent findings obtained in live, three-dimensional specimens using quantitative and mechanical approaches. Experiments in which overcrowding was induced in mouse neocortical NE/VZ, as well as comparisons of neocortical INM between mice and ferrets, have revealed that the behavior of NE/VZ cells can be affected by cellular densification. A consideration of the physical aspects in the NE/VZ and the mechanical difficulties associated with high-degree pseudostratification (PS) is important for achieving a better understanding of neocortical development and evolution.

No MeSH data available.