Nuclei as mechanical bumpers during epithelial remodeling

The morphogenesis of developing tissues relies on extensive cellular rearrangements in shape, position, and identity. A key process in reshaping tissues is cell intercalation-driven elongation, where epithelial cells align and intercalate along a common axis. Typically, analyses focus on how peripheral cortical forces influence cell shape changes. Less attention is given to how inhomogeneities in internal structures, particularly the nucleus, impact cell shaping. Here, we examine how pulsed contractile and extension dynamics interact with the nucleus in elongating Drosophila embryos. Our data show that tightly packed nuclei in apical layers hinder tissue remodeling/oscillatory behaviors. We identify two mechanisms for resolving internuclear tensions: nuclear deformation and dispersion. Embryos with non-deformable nuclei use nuclear dispersion to maintain near-normal extensile rates, while those with non-dispersible nuclei due to microtubule inhibition exhibit disruptions in contractile behaviors. Disrupting both mechanisms leads to severe tissue extension defects and cell extrusion. These findings highlight the critical role of nuclear shape and positioning in topological remodeling of epithelia.

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Publication Details

Journal
The Journal of Cell Biology
Published
2024-09-26
DOI
https://doi.org/10.1083/jcb.202405078
Citations
9
Primary Topic
Cellular Mechanics and Interactions
Type
article
Field-Weighted Citation Impact
2.93

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article

Nuclei as mechanical bumpers during epithelial remodeling

Rashmi Budhathoki, Dinah Loerke, J. Todd Blankenship, Noah F. de Leeuw et al.
9 citations
The Journal of Cell Biology
Cellular Mechanics and Interactions
2.93
article

Nuclei as mechanical bumpers during epithelial remodeling

Rashmi Budhathoki, Dinah Loerke, J. Todd Blankenship, Noah F. de Leeuw, Liam J. Russell
article en
9 citations

Abstract

The morphogenesis of developing tissues relies on extensive cellular rearrangements in shape, position, and identity. A key process in reshaping tissues is cell intercalation-driven elongation, where epithelial cells align and intercalate along a common axis. Typically, analyses focus on how peripheral cortical forces influence cell shape changes. Less attention is given to how inhomogeneities in internal structures, particularly the nucleus, impact cell shaping. Here, we examine how pulsed contractile and extension dynamics interact with the nucleus in elongating Drosophila embryos. Our data show that tightly packed nuclei in apical layers hinder tissue remodeling/oscillatory behaviors. We identify two mechanisms for resolving internuclear tensions: nuclear deformation and dispersion. Embryos with non-deformable nuclei use nuclear dispersion to maintain near-normal extensile rates, while those with non-dispersible nuclei due to microtubule inhibition exhibit disruptions in contractile behaviors. Disrupting both mechanisms leads to severe tissue extension defects and cell extrusion. These findings highlight the critical role of nuclear shape and positioning in topological remodeling of epithelia.

The Journal of Cell BiologyVol. 223(12)
University of Denver (US)
National Institutes of Health, National Institute of General Medical Sciences
Openalex Percentile: Top 9%
Cellular Mechanics and Interactions
2.93
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Nuclei as mechanical bumpers during epithelial remodeling — Rashmi Budhathoki, Dinah Loerke, et al. · The Journal of Cell Biology (2024) | TGRS Research Map | TGRS