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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.


Related in: MedlinePlus

Summary of acute TAG-1–knockdown (KD) experiments (Okamoto et al., 2013). TAG-1 shRNA was introduced through in utero electroporation at mouse embryonic day 10 (E10). By E12, VZ cells lost basal processes and were overcrowded near the apical surface. By E13, they detached from the apical surface and invaded the basal neuronal territory. The delaminated progenitors then heterotopically divided, generating different classes of neurons. Initial intermingling of neurons and progenitors (E13) and subsequent ectopic neuron production (~E17) disrupted neuronal layer formation, resulting in a mosaic-like abnormal distribution pattern.
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Figure 5: Summary of acute TAG-1–knockdown (KD) experiments (Okamoto et al., 2013). TAG-1 shRNA was introduced through in utero electroporation at mouse embryonic day 10 (E10). By E12, VZ cells lost basal processes and were overcrowded near the apical surface. By E13, they detached from the apical surface and invaded the basal neuronal territory. The delaminated progenitors then heterotopically divided, generating different classes of neurons. Initial intermingling of neurons and progenitors (E13) and subsequent ectopic neuron production (~E17) disrupted neuronal layer formation, resulting in a mosaic-like abnormal distribution pattern.

Mentions: If inherited basal processes are strictly analogs to priority boarding passes that streamline the flow of passengers under crowded conditions, the loss of these processes should lead to traffic problems such as severe overcrowding and congestion. Acute knockdown (KD) of the cell-surface molecule TAG-1 was used to determine the functional importance of the basal process and address the role of normal INM in overall brain formation (Okamoto et al., 2013). Upon loss of TAG-1, which is normally expressed in the basal part of mouse neocortical walls at embryonic day 10 (E10)–E11, VZ cells lost their basal processes by E12. Consequently, their basalward nucleokinesis was severely limited, causing their somata to accumulate near the apical surface (Figure 5, left part). By E13, these abnormally shortened VZ cells delaminated from the apical surface and invaded the basal area that should normally be occupied by neurons, thereby disrupting segregation of progenitor cells and neurons (Figure 5, center). The delaminated progenitors remained proliferative/undifferentiated (Pax6+) at heterotopic (far basal) positions until late in embryonic development (~E17). Nevertheless, distribution of neurons that were generated sequentially from these malpositioned progenitors was quite abnormal. Instead of forming layers, ectopically generated neurons were scattered almost throughout the wall in a randomized pattern (Figure 5, right part). This dysplasia therefore indicates that appropriate control of nucleokinesis within the early NE/VZ is important for preventing intermingling of progenitors and neurons, and thereby contributes to normal brain formation. However, why do the acutely shortened VZ cells in TAG-1–KD cerebral walls observed at E12 detach from the apical surface by E13?


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)

Summary of acute TAG-1–knockdown (KD) experiments (Okamoto et al., 2013). TAG-1 shRNA was introduced through in utero electroporation at mouse embryonic day 10 (E10). By E12, VZ cells lost basal processes and were overcrowded near the apical surface. By E13, they detached from the apical surface and invaded the basal neuronal territory. The delaminated progenitors then heterotopically divided, generating different classes of neurons. Initial intermingling of neurons and progenitors (E13) and subsequent ectopic neuron production (~E17) disrupted neuronal layer formation, resulting in a mosaic-like abnormal distribution pattern.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Summary of acute TAG-1–knockdown (KD) experiments (Okamoto et al., 2013). TAG-1 shRNA was introduced through in utero electroporation at mouse embryonic day 10 (E10). By E12, VZ cells lost basal processes and were overcrowded near the apical surface. By E13, they detached from the apical surface and invaded the basal neuronal territory. The delaminated progenitors then heterotopically divided, generating different classes of neurons. Initial intermingling of neurons and progenitors (E13) and subsequent ectopic neuron production (~E17) disrupted neuronal layer formation, resulting in a mosaic-like abnormal distribution pattern.
Mentions: If inherited basal processes are strictly analogs to priority boarding passes that streamline the flow of passengers under crowded conditions, the loss of these processes should lead to traffic problems such as severe overcrowding and congestion. Acute knockdown (KD) of the cell-surface molecule TAG-1 was used to determine the functional importance of the basal process and address the role of normal INM in overall brain formation (Okamoto et al., 2013). Upon loss of TAG-1, which is normally expressed in the basal part of mouse neocortical walls at embryonic day 10 (E10)–E11, VZ cells lost their basal processes by E12. Consequently, their basalward nucleokinesis was severely limited, causing their somata to accumulate near the apical surface (Figure 5, left part). By E13, these abnormally shortened VZ cells delaminated from the apical surface and invaded the basal area that should normally be occupied by neurons, thereby disrupting segregation of progenitor cells and neurons (Figure 5, center). The delaminated progenitors remained proliferative/undifferentiated (Pax6+) at heterotopic (far basal) positions until late in embryonic development (~E17). Nevertheless, distribution of neurons that were generated sequentially from these malpositioned progenitors was quite abnormal. Instead of forming layers, ectopically generated neurons were scattered almost throughout the wall in a randomized pattern (Figure 5, right part). This dysplasia therefore indicates that appropriate control of nucleokinesis within the early NE/VZ is important for preventing intermingling of progenitors and neurons, and thereby contributes to normal brain formation. However, why do the acutely shortened VZ cells in TAG-1–KD cerebral walls observed at E12 detach from the apical surface by E13?

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.


Related in: MedlinePlus