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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.


Pseudostratification of epithelial cells achieved through interkinetic nuclear migration.
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Figure 1: Pseudostratification of epithelial cells achieved through interkinetic nuclear migration.

Mentions: The neural tube and walls of the early embryonic brain vesicles are composed entirely of undifferentiated progenitor cells (or “matrix cells” (Fujita, 1963)) and are referred to collectively as the neuroepithelium (NE) (reviewed in Götz and Huttner, 2005; Miyata, 2008; Taverna et al., 2014). Structurally, the NE is pseudostratified; that is, although there are several layers of nuclei in the NE wall (Figure 1, left), one layer of cells can host multiple layers of nuclei (Figure 1, right). Each cell extends to contact both the apical and basal surfaces of the wall, resulting in a bipolar cellular morphology with apical and basal processes. Nuclei of progenitor cells born at the apical surface of the NE move toward the basal side of the NE during G1 phase of the cell cycle. After completing S-phase in the basal portion of the NE, the nuclei return to the apical surface, where they undergo division as their parent cells did. Collectively, these processes are referred to as interkinetic nuclear migration, INM (or IKNM), (Schaper, 1897; Sauer, 1935; Sauer and Walker, 1959; Sidman et al., 1959; Fujita, 1962, reviewed in Taverna and Huttner, 2010; Kosodo, 2012; Reiner et al., 2012; Spear and Erickson, 2012; Lee and Norden, 2013).


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)

Pseudostratification of epithelial cells achieved through interkinetic nuclear migration.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Pseudostratification of epithelial cells achieved through interkinetic nuclear migration.
Mentions: The neural tube and walls of the early embryonic brain vesicles are composed entirely of undifferentiated progenitor cells (or “matrix cells” (Fujita, 1963)) and are referred to collectively as the neuroepithelium (NE) (reviewed in Götz and Huttner, 2005; Miyata, 2008; Taverna et al., 2014). Structurally, the NE is pseudostratified; that is, although there are several layers of nuclei in the NE wall (Figure 1, left), one layer of cells can host multiple layers of nuclei (Figure 1, right). Each cell extends to contact both the apical and basal surfaces of the wall, resulting in a bipolar cellular morphology with apical and basal processes. Nuclei of progenitor cells born at the apical surface of the NE move toward the basal side of the NE during G1 phase of the cell cycle. After completing S-phase in the basal portion of the NE, the nuclei return to the apical surface, where they undergo division as their parent cells did. Collectively, these processes are referred to as interkinetic nuclear migration, INM (or IKNM), (Schaper, 1897; Sauer, 1935; Sauer and Walker, 1959; Sidman et al., 1959; Fujita, 1962, reviewed in Taverna and Huttner, 2010; Kosodo, 2012; Reiner et al., 2012; Spear and Erickson, 2012; Lee and Norden, 2013).

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.