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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.


A traffic bottleneck problem that presumably exists subapically in the ventricular zone (VZ) in the presence of high-degree pseudostratification (PS). The left panel shows a highly pseudostratified VZ; a horizontally dividing M-phase cell is colored in green, and the apical junction meshwork is colored in magenta. In the right panel, the space that the voluminous (expanding) M-phase cell inevitably occupies and the space through which its daughter cells must pass are compared. The latter space (outflow tract) may be much smaller due to VZ densification.
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Figure 3: A traffic bottleneck problem that presumably exists subapically in the ventricular zone (VZ) in the presence of high-degree pseudostratification (PS). The left panel shows a highly pseudostratified VZ; a horizontally dividing M-phase cell is colored in green, and the apical junction meshwork is colored in magenta. In the right panel, the space that the voluminous (expanding) M-phase cell inevitably occupies and the space through which its daughter cells must pass are compared. The latter space (outflow tract) may be much smaller due to VZ densification.

Mentions: This discussion should be coupled with consideration of why NE/VZ progenitor cells divide at the apical surface. The centrosome is located in the apical endfoot due to the presence of a primary cilium (Paridaen et al., 2013; Insolera et al., 2014). Primary cilia are implicated in Wnt and Shh signaling as well as cell-cycle regulation (reviewed in Bisgrove and Yost, 2006; Fuccillo et al., 2006; Marshall and Nonaka, 2006), suggesting that progenitor cells need to possess an apical endfoot with a primary cilium in order to maintain their developmental potential and stem cell–like proliferation (Götz and Huttner, 2005; Cappello et al., 2006). Furthermore, the Delta–Notch interaction, which is important for the maintenance of stem-like cells, occurs at the apical surface (adherens junction) (Ohata et al., 2011; Hatakeyama et al., 2014). For undifferentiated NE/VZ cells connected to the apical surface, it seems beneficial to send the nucleus/soma to the apical endfoot in order to make the centrosome available for mitosis. Also, integration of newly generated daughter cells into the apical surface is easily achieved through apical mitoses. In the developing mouse neocortex, most apical mitoses occur with a cleavage furrow perpendicular to the apical surface, dividing each apical endfoot (Smart, 1973; Konno et al., 2008; Shitamukai and Matsuzaki, 2012; Figure 3). Consequently, daughter cells can easily and immediately join the apical meshwork. Thus, localizing mitoses to the apical surface is a favorable cytogenetic strategy for efficient expansion of undifferentiated NE/VZ cells in brain primordia. INM-mediated PS facilitates apical divisions, thereby supporting the maintenance/expansion of undifferentiated stem-like cells.


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)

A traffic bottleneck problem that presumably exists subapically in the ventricular zone (VZ) in the presence of high-degree pseudostratification (PS). The left panel shows a highly pseudostratified VZ; a horizontally dividing M-phase cell is colored in green, and the apical junction meshwork is colored in magenta. In the right panel, the space that the voluminous (expanding) M-phase cell inevitably occupies and the space through which its daughter cells must pass are compared. The latter space (outflow tract) may be much smaller due to VZ densification.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: A traffic bottleneck problem that presumably exists subapically in the ventricular zone (VZ) in the presence of high-degree pseudostratification (PS). The left panel shows a highly pseudostratified VZ; a horizontally dividing M-phase cell is colored in green, and the apical junction meshwork is colored in magenta. In the right panel, the space that the voluminous (expanding) M-phase cell inevitably occupies and the space through which its daughter cells must pass are compared. The latter space (outflow tract) may be much smaller due to VZ densification.
Mentions: This discussion should be coupled with consideration of why NE/VZ progenitor cells divide at the apical surface. The centrosome is located in the apical endfoot due to the presence of a primary cilium (Paridaen et al., 2013; Insolera et al., 2014). Primary cilia are implicated in Wnt and Shh signaling as well as cell-cycle regulation (reviewed in Bisgrove and Yost, 2006; Fuccillo et al., 2006; Marshall and Nonaka, 2006), suggesting that progenitor cells need to possess an apical endfoot with a primary cilium in order to maintain their developmental potential and stem cell–like proliferation (Götz and Huttner, 2005; Cappello et al., 2006). Furthermore, the Delta–Notch interaction, which is important for the maintenance of stem-like cells, occurs at the apical surface (adherens junction) (Ohata et al., 2011; Hatakeyama et al., 2014). For undifferentiated NE/VZ cells connected to the apical surface, it seems beneficial to send the nucleus/soma to the apical endfoot in order to make the centrosome available for mitosis. Also, integration of newly generated daughter cells into the apical surface is easily achieved through apical mitoses. In the developing mouse neocortex, most apical mitoses occur with a cleavage furrow perpendicular to the apical surface, dividing each apical endfoot (Smart, 1973; Konno et al., 2008; Shitamukai and Matsuzaki, 2012; Figure 3). Consequently, daughter cells can easily and immediately join the apical meshwork. Thus, localizing mitoses to the apical surface is a favorable cytogenetic strategy for efficient expansion of undifferentiated NE/VZ cells in brain primordia. INM-mediated PS facilitates apical divisions, thereby supporting the maintenance/expansion of undifferentiated stem-like cells.

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.