Tissue mechanics and systemic signaling safeguard epithelial tissue against spindle misorientation
Posted on: 26 January 2026 , updated on: 28 January 2026
Preprint posted on 19 October 2025
The threefold way an epithelium copes with cell misplacement: pulling them up, killing them less, and removing the unwanted.
Selected by Ruoheng Li
Categories: cell biology, developmental biology
Introduction
What would happen if we messed up mitotic spindle positioning in an epithelial monolayer?
Normally, cells need to place their spindle parallel to the epithelial sheet so that the two daughter cells remain inside the layer. Without proper spindle positioning, then, we would have a whole range of misoriented divisions, with daughter cells getting unequal apical areas, or even with one daughter cell not in the layer at all.
Surprisingly, knocking out the key spindle positioning factor NuMA in Drosophila would have little impact on development. So, some buffering mechanisms must be at work to fix misplaced cells and compensate for the unproductive divisions.
Here, using Drosophila pupal dorsal thorax epithelium (notum) as the experimental system, Floris Bosveld and colleagues explored how epithelial cell number remains robust against cell misplacements.
What I like about this preprint
I think this preprint gives a very systematic explanation about how the notum tissue maintains its cell number against cell misposition and loss, and it is interesting to learn that the innate properties of the epithelia – tissue-wide tension, regulation of apoptosis based on apical size – can directly buffer against a rather significant perturbation. On a more detailed level, I am particularly impressed by the experiments elucidating cell reintegration mechanisms: I find the laser ablation assay and the clonal disturbance of myosin activity very cleverly designed, concretely demonstrating the importance of local tensile forces while disentangling it from the contractility of the reintegrating cell itself.
Key findings
Fig. 1 Different outcomes of misoriented divisions in mud mutant notum tissue. Figure adapted from the preprint where it is available under a CC-BY-NC 4.0 International license.
- Loss of NuMA causes cell mispositioning and loss in the notum tissue
Loss of NuMA causes frequent spindle misorientation, with up to 40% of divisions showing strongly tilted spindles. In ~27% of cases, only one daughter cell remains within the tissue, while the other is displaced basally. The mispositioned daughter within the tissue can either reintegrate in a basal-to-apical manner or delaminate and undergo apoptosis.
- Cell reintegration does not depend on lateral adhesion but requires actomyosin-dependent pulling forces from neighboring cells
RNAi knockdown of septate junctions (SJs), tricellular junctions, or adhesion components did not significantly reduce the rate of cell reintegration. This distinguishes basal-to-apical reintegration in the notum from previously reported apical-to-basal reintegration mechanisms.
In contrast, reintegrating cells appear to experience pulling forces from their neighbors. The authors provide two lines of evidence: first, laser ablation of the reintegrating cell causes expansion of its apex, whereas ablation of neighboring cells causes it to shrink; second, live imaging shows that when a neighboring cell undergoes cytokinesis, constriction of the cytokinetic ring temporally accelerates reintegration, consistent with the reintegrating cell being pulled by its neighbors.
Fig 2. Laser ablation assay of either the reintegrating cell or its neighbours. Figure adapted from the preprint where it is available under a CC-BY-NC 4.0 International license.
The authors further show that this pulling force depends on actomyosin activity: global interference with myosin function (dominant-negative myosin overexpression or Rok knockdown) compromises cell reintegration.
Importantly, contractility in neighboring cells appears to matter more than that of the reintegrating cell itself. When dominant-negative myosin II was overexpressed clonally, reintegration at clone boundaries was slowed – despite the reintegrating cell itself not being perturbed.
Fig 3. In mud mutant tissue clonally expressing dominant negative myosin (zipDN), reintegration of mud cells facing mud zipDN cells is compromised. Figure adapted from the preprint where it is available under a CC-BY-NC 4.0 International license.
- Reduced apoptosis compensates for cell loss induced by mis-oriented division
Fig 4. Reduced apoptosis compensated for cell number loss in mud mutant notum. Figure adapted from the preprint where it is available under a CC-BY-NC 4.0 International license.
The authors next examine how cell loss is compensated. Under normal conditions, the notum undergoes two successive waves of cell division, with an increase in apoptosis following the first wave. In mud mutants, cell division rates remain comparable to controls, but apoptosis is strongly reduced after the first division wave, compensating for cell loss caused by severely misoriented divisions.
The authors propose that this compensation operates through a known link between cell apical area and apoptosis: Hippo/YAP activity scales with apical area, so that cells with larger apical surfaces, having a higher Hippo/YAP activity, would be less likely to undergo apoptosis.
Thus, following a highly misoriented division, the lone daughter cell remaining in the tissue retains an apical area comparable to that of the mother cell—approximately twice what it would normally have—leading to elevated Hippo/YAP activity and reduced apoptosis.
Supporting this model, the authors show that lone daughter cells indeed undergo apoptosis less frequently, and that perturbing the scaling between Hippo/YAP activity and apical area greatly increases apoptosis specifically in mud mutant tissue.
Fig 5. Lone daughters have higher ban3 levels and lower apoptosis rates. Figure adapted from the preprint where it is available under a CC-BY-NC 4.0 International license.
- Systemic TNF signaling eliminates basally displaced cells that fail to reintegrate
The second daughter cell produced by highly misoriented divisions is displaced beneath the tissue and eventually undergoes apoptosis. The TNF pathway, previously shown to eliminate polarity-deficient epithelial cells, is also required for the removal of these displaced cells: perturbation of TNF signaling strongly reduces apoptosis below the notum tissue.
However, this perturbation does not significantly affect cell numbers within the notum, suggesting that elimination of basally misplaced cells is not required for overall tissue cell number maintenance.
Questions to the authors
- For the cell reintegration mechanism: in your opinion, does the tensile force pulling the reintegrating cell up come more from its direct neighbours, or from tension across the whole tissue?
- For the lone daughter produced by highly misoriented divisions: what is happening on the basal side of these cells – presumably they would need to re-establish attachment to the basal membrane/ECM? Would this be related in any way to their apical dynamics, for instance the fact that it takes longer for them to adjust their apical area?
References
- Bergstralh DT, Lovegrove HE, St Johnston D. Lateral adhesion drives reintegration of misplaced cells into epithelial monolayers. Nat Cell Biol. 2015;17(11):1497-1503. doi:10.1038/ncb3248
- Cammarota C, Finegan TM, Wilson TJ, Yang S, Bergstralh DT. An Axon-Pathfinding Mechanism Preserves Epithelial Tissue Integrity. Curr Biol. 2020;30(24):5049-5057.e3. doi:10.1016/j.cub.2020.09.061
- López-Gay JM, Nunley H, Spencer M, et al. Apical stress fibers enable a scaling between cell mechanical response and area in epithelial tissue. Science. 2020;370(6514):eabb2169. doi:10.1126/science.ab
doi: https://doi.org/10.1242/prelights.42793
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