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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.


Basal process–mediated sequential basalward nucleokinesis by pair-generated sister cells. Each apically dividing M-phase cell’s basal process is maintained and inherited by one of its daughter cells (Miyata et al., 2001). The process-inheriting daughter cell exhibits quicker (more directional) basalward nuckeokinesis than its sister cell.
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Figure 4: Basal process–mediated sequential basalward nucleokinesis by pair-generated sister cells. Each apically dividing M-phase cell’s basal process is maintained and inherited by one of its daughter cells (Miyata et al., 2001). The process-inheriting daughter cell exhibits quicker (more directional) basalward nuckeokinesis than its sister cell.

Mentions: Time-lapse monitoring of daughter cells generated at the apical surface of VZ in slice culture was followed by quantitative analysis of nuclear movements. Measurement of mean-squared displacement (MSD) was used to determine the relationship between the morphology of daughter cells and the directionality of their initial nuclear movement. If the MSD for a tracked nucleus has a linear relationship with elapsed time (i.e., the MSD graph exhibits a linear pattern), the movement of the tested nucleus is considered to have random tendencies (i.e., non-directional and fluctuating motion). If the MSD graph instead exhibits a positive curvature, the movement is considered to be directional or persistent (Norden et al., 2009; Leung et al., 2011). The basal process of each apically dividing M-phase progenitor in the NE/VZ with a certain minimum thickness (>50 µm) is inherited by one of its daughters (Miyata et al., 2001; Noctor et al., 2001). In nuclear MSD profiles of daughter cells generated from a single progenitor, a more directional pattern was observed in the process-inheriting daughter cell than in its sister cell (Okamoto et al., 2013). This mechanism, in which the process-inheriting daughter cell moves its nucleus more quickly than its sister cell, is analogs to “priority boarding” in air travel or “staggered commuting” in metropolitan railway systems, and may contribute to the normally prompt stratification of nuclei/somata in each outflow tract (Figure 4).


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)

Basal process–mediated sequential basalward nucleokinesis by pair-generated sister cells. Each apically dividing M-phase cell’s basal process is maintained and inherited by one of its daughter cells (Miyata et al., 2001). The process-inheriting daughter cell exhibits quicker (more directional) basalward nuckeokinesis than its sister cell.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Basal process–mediated sequential basalward nucleokinesis by pair-generated sister cells. Each apically dividing M-phase cell’s basal process is maintained and inherited by one of its daughter cells (Miyata et al., 2001). The process-inheriting daughter cell exhibits quicker (more directional) basalward nuckeokinesis than its sister cell.
Mentions: Time-lapse monitoring of daughter cells generated at the apical surface of VZ in slice culture was followed by quantitative analysis of nuclear movements. Measurement of mean-squared displacement (MSD) was used to determine the relationship between the morphology of daughter cells and the directionality of their initial nuclear movement. If the MSD for a tracked nucleus has a linear relationship with elapsed time (i.e., the MSD graph exhibits a linear pattern), the movement of the tested nucleus is considered to have random tendencies (i.e., non-directional and fluctuating motion). If the MSD graph instead exhibits a positive curvature, the movement is considered to be directional or persistent (Norden et al., 2009; Leung et al., 2011). The basal process of each apically dividing M-phase progenitor in the NE/VZ with a certain minimum thickness (>50 µm) is inherited by one of its daughters (Miyata et al., 2001; Noctor et al., 2001). In nuclear MSD profiles of daughter cells generated from a single progenitor, a more directional pattern was observed in the process-inheriting daughter cell than in its sister cell (Okamoto et al., 2013). This mechanism, in which the process-inheriting daughter cell moves its nucleus more quickly than its sister cell, is analogs to “priority boarding” in air travel or “staggered commuting” in metropolitan railway systems, and may contribute to the normally prompt stratification of nuclei/somata in each outflow tract (Figure 4).

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.