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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.


Graphs depicting the relationship between the degree of pseudostratification (PS) and cell production at the apical surface (A, see also Figure 2), difficulties and INM modulation in high-degree PS (B), and a possible revolutionary change in the strategy for cell production from “PS-based apical” under physical/traffic limitations to “non-PS-mediated basal”, which is free from subapical traffic difficulties (C).
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Figure 9: Graphs depicting the relationship between the degree of pseudostratification (PS) and cell production at the apical surface (A, see also Figure 2), difficulties and INM modulation in high-degree PS (B), and a possible revolutionary change in the strategy for cell production from “PS-based apical” under physical/traffic limitations to “non-PS-mediated basal”, which is free from subapical traffic difficulties (C).

Mentions: As discussed in the first part of this review, PS is an important means by which an epithelial system can increase its productivity at the apical surface (Figures 2, 9A). The second part of this review discussed the difficulties of high-degree PS from the viewpoint of nuclear traffic (Figures 5, 6). The apical surface is contractile and thus always spontaneously narrowing, although it receives M-phase somata that are expanding and voluminous (Figure 3). The co-occurrence of these two mechanically opposing phenomena is supported by the quick disappearance of newly generated G1-phase daughter cells’ nuclei from the apical surface. The exclusive use of the mother (M-phase) cell’s basal process by only one of its daughter cells facilitates the initial sequential (and thus non-competitive) nucleokinesis of the pair-generated sister cells’ nuclei away from the subapical space (the third part of this review, Figures 4, 8). This mechanism may collaborate with other mechanisms reported for basalward nucleokinesis during G1-phase: actomyosin-dependent (Schenk et al., 2009) and microtubule-dependent (Tsai et al., 2010) intracellular regulation, as well as passive basalward nuclear movements dependent on the apicalward nucleokinesis of other cells (Sauer, 1935; Norden et al., 2009; Kosodo et al., 2011; Leung et al., 2011).


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)

Graphs depicting the relationship between the degree of pseudostratification (PS) and cell production at the apical surface (A, see also Figure 2), difficulties and INM modulation in high-degree PS (B), and a possible revolutionary change in the strategy for cell production from “PS-based apical” under physical/traffic limitations to “non-PS-mediated basal”, which is free from subapical traffic difficulties (C).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 9: Graphs depicting the relationship between the degree of pseudostratification (PS) and cell production at the apical surface (A, see also Figure 2), difficulties and INM modulation in high-degree PS (B), and a possible revolutionary change in the strategy for cell production from “PS-based apical” under physical/traffic limitations to “non-PS-mediated basal”, which is free from subapical traffic difficulties (C).
Mentions: As discussed in the first part of this review, PS is an important means by which an epithelial system can increase its productivity at the apical surface (Figures 2, 9A). The second part of this review discussed the difficulties of high-degree PS from the viewpoint of nuclear traffic (Figures 5, 6). The apical surface is contractile and thus always spontaneously narrowing, although it receives M-phase somata that are expanding and voluminous (Figure 3). The co-occurrence of these two mechanically opposing phenomena is supported by the quick disappearance of newly generated G1-phase daughter cells’ nuclei from the apical surface. The exclusive use of the mother (M-phase) cell’s basal process by only one of its daughter cells facilitates the initial sequential (and thus non-competitive) nucleokinesis of the pair-generated sister cells’ nuclei away from the subapical space (the third part of this review, Figures 4, 8). This mechanism may collaborate with other mechanisms reported for basalward nucleokinesis during G1-phase: actomyosin-dependent (Schenk et al., 2009) and microtubule-dependent (Tsai et al., 2010) intracellular regulation, as well as passive basalward nuclear movements dependent on the apicalward nucleokinesis of other cells (Sauer, 1935; Norden et al., 2009; Kosodo et al., 2011; Leung et al., 2011).

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.