Heterogeneity, Cell Biology and Tissue Mechanics of Pseudostratified Epithelia: Coordination of Cell Divisions and Growth in Tightly Packed Tissues

Strzyz, Paulina; Matejčić, Marija; Norden, Caren

doi:10.1016/bs.ircmb.2016.02.004

Cited by 51 publications

(59 citation statements)

References 75 publications

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“…However, the loss of Lgl1 causes a dramatic loss of polarity specifically in radial glia located in the ganglionic eminences , suggesting that there might be differences in polarity determinants between dorsal and ventral RG. These processes are kept throughout the cell cycle, during which RG perform an evolutionarily conserved movement known as interkinetic nuclear migration (INM), whereby their nuclei undergo S phase at the basal end of the VZ and mitosis at the ventricular surface, moving between these locations through G1 and G2 . The duration of the different phases of the cell cycle of subpallial progenitors could presumably play an important role in their expansion and the diversity of their neuronal output, as it does in the developing cortex .…”

Section: Cell Biology Of Ventral Radial Gliamentioning

confidence: 99%

Radial glia in the ventral telencephalon

García

Harwell

2017

FEBS Letters

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The ventral telencephalon is the developmental origin of the basal ganglia and the source of neuronal and glial cells that integrate into developing circuits in other areas of the brain. Radial glia in the embryonic subpallium give rise to an enormous diversity of mature cell types, either directly or through other transit-amplifying progenitors. Here, we review current knowledge about these subpallial neural stem cells and their progeny, focusing on the period of neurogenesis. We describe their cell biological features and the extrinsic and intrinsic molecular codes that guide their fate specification in defined temporal and spatial sequences. We also discuss the role of clonal lineage in the organization and specification of mature neurons.

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Section: Cell Biology Of Ventral Radial Gliamentioning

confidence: 99%

Radial glia in the ventral telencephalon

García

Harwell

2017

FEBS Letters

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“…This finding suggests that proliferative cells may sense and respond to excessive mechanical stress generated in the subapical space. It also raises the possibility that similar sensing and responses to mechanical factors might also occur under physiological (non-overcrowded) conditions, possibly coordinating heterogeneous nuclear and somal movements (Miyata et al, 2015; Strzyz et al, 2016). We chose to focus on a microzone near (~10 μm from) the apical surface, where multiple mechanical events, such as mitosis, resultant duplication of nuclear and somal flow, as well as apical constriction, take place.…”

Section: Introductionmentioning

confidence: 99%

Differences in the Mechanical Properties of the Developing Cerebral Cortical Proliferative Zone between Mice and Ferrets at both the Tissue and Single-Cell Levels

Nagasaka

Shinoda

Kawaue

et al. 2016

Front. Cell Dev. Biol.

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Cell-producing events in developing tissues are mechanically dynamic throughout the cell cycle. In many epithelial systems, cells are apicobasally tall, with nuclei and somata that adopt different apicobasal positions because nuclei and somata move in a cell cycle–dependent manner. This movement is apical during G2 phase and basal during G1 phase, whereas mitosis occurs at the apical surface. These movements are collectively referred to as interkinetic nuclear migration, and such epithelia are called “pseudostratified.” The embryonic mammalian cerebral cortical neuroepithelium is a good model for highly pseudostratified epithelia, and we previously found differences between mice and ferrets in both horizontal cellular density (greater in ferrets) and nuclear/somal movements (slower during G2 and faster during G1 in ferrets). These differences suggest that neuroepithelial cells alter their nucleokinetic behavior in response to physical factors that they encounter, which may form the basis for evolutionary transitions toward more abundant brain-cell production from mice to ferrets and primates. To address how mouse and ferret neuroepithelia may differ physically in a quantitative manner, we used atomic force microscopy to determine that the vertical stiffness of their apical surface is greater in ferrets (Young's modulus = 1700 Pa) than in mice (1400 Pa). We systematically analyzed factors underlying the apical-surface stiffness through experiments to pharmacologically inhibit actomyosin or microtubules and to examine recoiling behaviors of the apical surface upon laser ablation and also through electron microscopy to observe adherens junction. We found that although both actomyosin and microtubules are partly responsible for the apical-surface stiffness, the mouse

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“…To understand the different forces that drive apical nuclear migration in hindbrain and retina, we probed the cytoskeletal elements involved in their generation. In pseudostratified epithelia these forces have been shown to be generated by microtubules (Hu et al, 2013;Shu et al, 2004;Strzyz et al, 2016;Tsai et al, 2010) or actomyosin (Meyer et al, 2011;Norden et al, 2009). While it is known that in retinal neuroepithelia apical nuclear migration is actomyosin-dependent (Norden et al, 2009;Strzyz et al, 2015), the cytoskeletal elements that move nuclei in hindbrain neuroepithelia were yet unspecified.…”

Section: Distinct Actomyosin Pools Are Involved In Nuclear Movements mentioning

confidence: 99%

“…If nuclei fail to position apically, divisions occur at basal locations and these basally dividing cells perturb epithelial integrity and maturation (Strzyz et al, 2015). Interestingly, the cytoskeletal elements responsible for this crucial apical nuclear positioning differ depending on epithelium (Lee and Norden, 2013;Norden, 2017;Strzyz et al, 2016). In the extremely elongated cells of the rodent neocortex, movements are microtubuledependent (Bertipaglia et al, 2017) and the mechanisms have been extensively studied (Hu et al, 2013;Shu et al, 2004;Tsai et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…In the extremely elongated cells of the rodent neocortex, movements are microtubuledependent (Bertipaglia et al, 2017) and the mechanisms have been extensively studied (Hu et al, 2013;Shu et al, 2004;Tsai et al, 2010). In contrast, in shorter neuroepithelia nuclear positioning is driven by the actin cytoskeleton (Strzyz et al, 2016). However, the mechanisms by which actin generates the forces required for apical nuclear movement are still not fully understood.…”

Section: Introductionmentioning

confidence: 99%

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Tissue shape determines actin-dependent nuclear migration mechanisms in neuroepithelia

Yanakieva

Erzberger

Matejčić

et al. 2019

Preprint

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Correct nuclear position is crucial for cellular function and tissue development.Depending on cell context however, cytoskeletal elements responsible for nuclear positioning vary. While these cytoskeletal mechanisms have been intensely studied in single cells, how nuclear positioning is linked to tissue morphology is less clear.Here, we compare apical nuclear positioning in zebrafish neuroepithelia. We find that kinetics and actin-dependent mechanisms of nuclear positioning vary in tissues of different morphology. In straight neuroepithelia nuclear positioning is controlled by Rho-ROCK-dependent myosin contractility. In contrast, in basally constricted neuroepithelia a novel formin-dependent pushing mechanism is found for which we propose a proof-of-principle force generation theory.Overall, our data suggests that correct nuclear positioning is ensured by the adaptability of the cytoskeleton to cell and tissue shape. This in turn leads to robust epithelial maturation across geometries. The conclusion that different nuclear positioning mechanisms are favoured in tissues of different morphology highlights the importance of developmental context for the execution of intracellular processes.

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Heterogeneity, Cell Biology and Tissue Mechanics of Pseudostratified Epithelia: Coordination of Cell Divisions and Growth in Tightly Packed Tissues

Cited by 51 publications

References 75 publications

Radial glia in the ventral telencephalon

Radial glia in the ventral telencephalon

Differences in the Mechanical Properties of the Developing Cerebral Cortical Proliferative Zone between Mice and Ferrets at both the Tissue and Single-Cell Levels

Tissue shape determines actin-dependent nuclear migration mechanisms in neuroepithelia

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