Limits...
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.


Schematic illustrations depicting apicalward and basalward INM patterns and their differences between mice and ferrets (Okamoto et al., 2014).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4309187&req=5

Figure 8: Schematic illustrations depicting apicalward and basalward INM patterns and their differences between mice and ferrets (Okamoto et al., 2014).

Mentions: In the mouse neocortical VZ, apicalward nuclear movements exhibited by G2-phase progenitors are highly directional (i.e., quick and persistent until they reach the apical surface), with non-linear MSD profiles (Okamoto et al., 2013), very similar to the directional apicalward nuckeokinesis observed in zebrafish retina and brain stem (Norden et al., 2009; Leung et al., 2011). By contrast, the basalward nucleokinesis exhibited by G1-phase mouse VZ cells is less directional (i.e., nuclei exhibited non-linear MSD profiles along the apicobasal axis), as is also the case for zebrafish cells (Norden et al., 2009; Leung et al., 2011). As mentioned earlier, initial basalward nucleokinesis is more directional in daughter cells that inherit the basal process (“BP”) than in daughter cells that do not (“nonBP”) (Okamoto et al., 2013; Figure 4). Accordingly, the directionality of nucleokinesis in the mouse neocortical VZ is ranked in the following order: apicalward > BP-basalward > nonBP-basalward (Figure 8, upper panel). Surprisingly, MSD analysis of ferrets revealed that directionality in the mid-embryonic ferret neocortical VZ is ranked in a different order: BP-basalward > nonBP-basalward > apicalward (Okamoto et al., 2014; Figure 8, lower panel). This finding suggests that although the basal process–mediated mechanism for differential initiation of nucleokinesis (Okamoto et al., 2013) is conserved between mice and ferrets, strategies for balancing flows to and from the apical surface differ between these species. Ferret–mouse comparisons at each phase of nucleokinesis suggested that the basalward phase is relatively accelerated, whereas the apicalward phase is decelerated, in ferrets. Future studies should investigate the molecular mechanisms underlying these differential nucleokinesis patterns between mice and ferrets. Whether physical conditions (such as elasticity or stiffness) vary between VZs of different nuclear density could be assessed quantitatively using atomic force microscopic (AFM) techniques (Iwashita et al., 2014).


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)

Schematic illustrations depicting apicalward and basalward INM patterns and their differences between mice and ferrets (Okamoto et al., 2014).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 8: Schematic illustrations depicting apicalward and basalward INM patterns and their differences between mice and ferrets (Okamoto et al., 2014).
Mentions: In the mouse neocortical VZ, apicalward nuclear movements exhibited by G2-phase progenitors are highly directional (i.e., quick and persistent until they reach the apical surface), with non-linear MSD profiles (Okamoto et al., 2013), very similar to the directional apicalward nuckeokinesis observed in zebrafish retina and brain stem (Norden et al., 2009; Leung et al., 2011). By contrast, the basalward nucleokinesis exhibited by G1-phase mouse VZ cells is less directional (i.e., nuclei exhibited non-linear MSD profiles along the apicobasal axis), as is also the case for zebrafish cells (Norden et al., 2009; Leung et al., 2011). As mentioned earlier, initial basalward nucleokinesis is more directional in daughter cells that inherit the basal process (“BP”) than in daughter cells that do not (“nonBP”) (Okamoto et al., 2013; Figure 4). Accordingly, the directionality of nucleokinesis in the mouse neocortical VZ is ranked in the following order: apicalward > BP-basalward > nonBP-basalward (Figure 8, upper panel). Surprisingly, MSD analysis of ferrets revealed that directionality in the mid-embryonic ferret neocortical VZ is ranked in a different order: BP-basalward > nonBP-basalward > apicalward (Okamoto et al., 2014; Figure 8, lower panel). This finding suggests that although the basal process–mediated mechanism for differential initiation of nucleokinesis (Okamoto et al., 2013) is conserved between mice and ferrets, strategies for balancing flows to and from the apical surface differ between these species. Ferret–mouse comparisons at each phase of nucleokinesis suggested that the basalward phase is relatively accelerated, whereas the apicalward phase is decelerated, in ferrets. Future studies should investigate the molecular mechanisms underlying these differential nucleokinesis patterns between mice and ferrets. Whether physical conditions (such as elasticity or stiffness) vary between VZs of different nuclear density could be assessed quantitatively using atomic force microscopic (AFM) techniques (Iwashita et al., 2014).

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.