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Mechanical forces across compartments coordinate cell shape and fate transitions to generate tissue architecture

Clémentine Villeneuve, Ali Hashmi, Irene Ylivinkka, Elizabeth Lawson-Keister, Yekaterina A. Miroshnikova, Carlos Pérez-González, Bhagwan Yadav, Tao Zhang, Danijela Matic Vignjevic, Marja L. Mikkola, M. Lisa Manning, Sara A. Wickström

Posted on: 15 February 2023

Preprint posted on 12 December 2022

Article now published in Nature Cell Biology at http://dx.doi.org/10.1038/s41556-023-01332-4

It takes two to tango: coordinated mechanical contributions from epithelium and dermal fibroblasts help break symmetry for downgrowth and fate patterns in mouse hair follicles.

Selected by Sudeepa Nandi

 

Background:

The complex process of organ morphogenesis involves multiple modes of cell behavioural change and tissue deformation to enable an organ to achieve its functional form. However, it is unclear how different cell and tissue transformations are coordinated spatiotemporally to contribute to the specific cell states associated with organogenesis. This preprint investigates this fundamental question using the mouse hair follicle system.

The mammalian skin is adorned with periodically aligned hair follicles (HFs), which are complicated anatomic structures, comparable to mini-organs, constituting cells from different origins. These HFs are primarily composed of epithelial cells, originally derived from the surface epithelium (epidermis), dermal papilla cells that are derived from mesenchymal fibroblast cells in the dermis, and bulge stem cells. Bidirectional Wnt/ β-catenin pathway signaling between the epithelium and the underlying dermal layer helps establish the spatial alignment and molecular identity of the HF preplacodal cells within the initially homogeneous surface epithelial layer [1-4]. Simultaneously, the physical differences between the placodal cells and the other epidermal cells, arising after cellular rearrangements and compaction, become visible and the dermal fibroblasts cluster to form dermal condensate [5-7]. Also, Sox9, the master regulator for the adult HF stem cell niche, gets localized within the placodal confinement at E14.5 [8]. Then by E15.5, after an unknown trigger, the placodes invaginate to form hair follicle buds.

Although many groups have been working towards a better understanding of the underlying mechanisms, there are several questions still unanswered related to HF morphogenesis, such as (among others): 1) how the multi-layered placodal thickening emerges from the preplacodal state in the post-induction phase, 2) what regulates the Sox9 zonal restriction, 3) the physical mechanisms behind the invagination of the placodal thickening for bud formation. This study addresses some of these unresolved questions and provides a mechanistic insight into how cooperative cellular transformations within the epidermis and dermal fibroblasts allows symmetry breaking enabling pre-patterned epithelial placodes to achieve out-of-plane flow and fate patterning.

 

Key findings:

1) For a detailed characterization of cellular deformations in the epidermis, Villeneuve and colleagues used quantitative morphometric analysis and showed that the placodal cells elongate longitudinally towards the dermis in a volume-preserving manner. This elongation takes place only at E14.5, but is not observed at E13.5.

2) Through visual observations and examining tissue flows using particle image velocimetry (PIV), the authors further reported a collective in-plane oscillation and tissue flow within the epithelium at E14.5. On performing a circular laser cut around the placode neck, recoil could be observed directed outwards from the cut, confirming that the placode is under tension. However, as the contractile oscillations persisted at E15.5, the tissue flow shifted downwards driving elongation.

3) Phosphorylated myosin light chain-2 (pMLC2) staining intensity was higher in the apical domain of epidermal cells, however, the overall distribution within the placode was lower than that in the non-placodal epidermal cells.

4) Additionally, the dermal fibroblasts aggregated in a ring-like pattern around the base of the placodal thickening, corresponding to the region of observed in-plane oscillations.

5) Next, using 3D vertex modeling and comparative analysis, the authors found that while intrinsic forces were sufficient to drive cell elongation and curvature at E14.5, extrinsic forces were necessary at E15.5 to achieve the experimentally observed deformations. This suggested cooperation between intrinsic and extrinsic forces is essential for hair follicle placode development.

6) To confirm this, the authors performed genetic manipulations to investigate the role of myosin-IIA (Myh9), in the epidermis and the dermal fibroblasts separately, on mouse hair follicle placode development. They found that on knocking out myosin-IIA in the epidermis although placode development initiated without any changes in the isotropic elongation at E14.5, it led to less invagination and a reduced number of Sox9+ cells in the placodes at E15.5. The dermal condensate, that is the specialized fibroblast population, was found partially embedded within the placode in the epidermal-Myh9 KO. Meanwhile, knocking out myosin-IIA in dermal fibroblasts resulted in fewer placodes with less elongation and a reduced number of Sox9+ cells, particularly within the placodal region.

In addition, external static compression on organoids (with E14.5 epidermal progenitor cells) in 3D hydrogel was shown to induce Sox9 expression.

The above results collectively confirmed that the cellular deformations associated with placode invagination and pushing of the dermal condensate are driven by changes in contractility-mediated epidermal interfacial tension. But the full-scale morphogenetic transformation of the placode, along with Sox9 compartmentalization within them, needs additional contributions from the extrinsic contractile forces generated by the dermal fibroblast ring around the placode base.

7) This study also found that at E14.5, there were fewer cell divisions in the placodes compared to the epidermal cells and that at E15.5, most basal placodal cells rapidly divided. This corresponded with the nuclear inactivation and re-activation of YAP in the placode respectively at E14.5 and E15.5. On treating skin explants with Mitomycin-C, halting cell divisions, reduced the extent of budding, indicating that YAP activation and re-entry into cell division controls placodal downflow at E15.5.

8) The re-entry of the placodal cell cycle was enabled by the release of mechanical stress from confinement. At E14.5 the basement of the placodes had lower stiffness compared to the surrounding epidermis, which softened further at E15.5, as seen by AFM microscopy. This reduction in stiffness corresponded to high expression of MMPs in the dermal fibroblasts and placodes. Blocking the proteolytic degradation of the ECM in skin explants reduced the size and budding of placodes, indicating that the mechanical pressure release by ECM remodeling via MMP-mediated degradation is necessary for placodal budding. The results suggest that oriented cell divisions, enabled by stress release due to basement membrane remodeling, control placodal downward flow.

 

Why I like this preprint:

I have chosen this preprint for multiple reasons. This work has beautifully explored the combinatorial power of experimental biology and modeling to bring new insights into the process of mouse hair follicle morphogenesis. Their key observations, including how both crosstalks between epithelial and mesenchymal dynamics and the morphogenetic principles involving interplays between pressure, cellular shape changes, division, rearrangements, etc. for tissue deformations and flow, are valuable for the general biological and biophysical community. Importantly, 1) this has similarities to many cancer models which involve mechanical interactions with the surrounding mesenchymal fibroblasts, and 2) it allows us to better understand the fundamental basis of HFs for successful bioengineering applications such as building skin tissues.

 

Questions:

1) It is noteworthy to observe that, at E14.5 in Myh9-eKO mice, the placode cells did not show any elongation defects, despite the in-plane oscillations and the model suggesting that autonomous forces from polarized myosin distribution are important at E14.5. Can you provide an explanation for this observation?

2) I was wondering whether there were any early effects on compaction and rearrangement of placodal cells in Myh9-eKO? If so, can the Sox9 phenotype be a result of that? Did you see the ring arrangement of fibroblasts altered in Myh9-eKO mice, besides getting embedded in the placode cells?

3) You mentioned that in Myh9-dKO mice, the number of placodes was reduced. Could this also mean that the initial induction process is affected by this perturbation? or only that the morphologically identifiable changes are not occurring?

4) Can the experiment where you compress organoids be performed using epidermal progenitor cells from E14.5 Myh9-dKO mice?

5) Did you observe changes in placodal cell divisions/numbers after blocking MMP activity in dermal fibroblasts? Knowing the complex interplay between MMPs and YAP, would you want to dissect the sequence of their activations?

 

References:

[1] Biggs, L. C., & Mikkola, M. L. (2014). Early inductive events in ectodermal appendage morphogenesis. Seminars in cell & developmental biology, 25-26, 11–21. https://doi.org/10.1016/j.semcdb.2014.01.007

[2] Schmidt-Ullrich, R., & Paus, R. (2005). Molecular principles of hair follicle induction and morphogenesis. BioEssays: news and reviews in molecular, cellular and developmental biology, 27(3), 247–261. https://doi.org/10.1002/bies.20184

[3] Andl, T., Reddy, S. T., Gaddapara, T., & Millar, S. E. (2002). WNT signals are required for the initiation of hair follicle development. Developmental cell, 2(5), 643–653. https://doi.org/10.1016/s1534-5807(02)00167-3

[4] Saxena, N., Mok, K. W., & Rendl, M. (2019). An updated classification of hair follicle morphogenesis. Experimental dermatology, 28(4), 332–344. https://doi.org/10.1111/exd.13913

[5] Ahtiainen, L., Lefebvre, S., Lindfors, P. H., Renvoisé, E., Shirokova, V., Vartiainen, M. K., Thesleff, I., & Mikkola, M. L. (2014). Directional cell migration, but not proliferation, drives hair placode morphogenesis. Developmental cell, 28(5), 588–602. https://doi.org/10.1016/j.devcel.2014.02.003

[6] Biggs, L. C., Mäkelä, O. J., Myllymäki, S. M., Das Roy, R., Närhi, K., Pispa, J., Mustonen, T., & Mikkola, M. L. (2018). Hair follicle dermal condensation forms via Fgf20 primed cell cycle exit, cell motility, and aggregation. eLife, 7, e36468. https://doi.org/10.7554/eLife.36468

[7] Glover, J. D., Wells, K. L., Matthäus, F., Painter, K. J., Ho, W., Riddell, J., Johansson, J. A., Ford, M. J., Jahoda, C. A. B., Klika, V., Mort, R. L., & Headon, D. J. (2017). Hierarchical patterning modes orchestrate hair follicle morphogenesis. PLoS biology, 15(7), e2002117. https://doi.org/10.1371/journal.pbio.2002117

[8] Morita, R., Sanzen, N., Sasaki, H., Hayashi, T., Umeda, M., Yoshimura, M., Yamamoto, T., Shibata, T., Abe, T., Kiyonari, H., Furuta, Y., Nikaido, I., & Fujiwara, H. (2021). Tracing the origin of hair follicle stem cells. Nature, 594(7864), 547–552. https://doi.org/10.1038/s41586-021-03638-5

 

Tags: morphogenesis, mouse hair follicle, placode, stem cells, tissue deformation, tissue flow

doi: https://doi.org/10.1242/prelights.33688

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Authors' response

Clémentine Villeneuve and Elizabeth Lawson-Keister shared

Q1: It is noteworthy to observe that, at E14.5 in Myh9-eKO mice, the placode cells did not show any elongation defects, despite the in-plane oscillations and the model suggesting that autonomous forces from polarized myosin distribution are important at E14.5. Can you provide an explanation for this observation?

A: Indeed, the vertex model predicts that cell autonomous changes in surface tension could be sufficient to generate some degree of cell elongation and placode invagination at E14.5. However, our detailed analysis on the distribution of epidermal myosin activity showed that it is restricted to the apical surface and suprabasal layers of the epidermis. Such myosin distribution would be predicted to generate apical constriction, which we do not observe, indicating that non-epidermal forces counteract epidermal myosin. This notion is supported by the strong phenotype of the dermal Myh9 knockout, leading us to conclude that the in-plane oscillations are likely generated by contractile forces from the fibroblasts. We also have live imaging data from fibroblasts to support this. Of course, it is also possible that other cellular machineries, such as polarized distribution of cell adhesion components, could contribute to cell-autonomous changes in tension and thus cell shape within the epidermis, which will be interesting to study in the future.

Q2: I was wondering whether there were any early effects on compaction and rearrangement of placodal cells in Myh9-eKO? If so, can the Sox9 phenotype be a result of that? Did you see the ring arrangement of fibroblasts altered in Myh9-eKO mice, besides getting embedded in the placode cells?

A: This is a great question. A challenge in genetic studies of the epidermis is that the activity of the available efficient Cre lines such as the Keratin-14 Cre results in full absence of the deleted proteins only at E13-E14. We did not observe any substantial compaction defects in the placode and the surrounding epidermis, but it could be that the deletion of Myosin-IIA was not complete at E13. Also, the ring of fibroblasts was not affected, indicating that the assembly of the ring is most likely regulated by signalling crosstalk between the epidermis and the dermis, as is known for the dermal condensate.

Q3: You mentioned that in Myh9-dKO mice, the number of placodes was reduced. Could this also mean that the initial induction process is affected by this perturbation? or only that the morphologically identifiable changes are not occurring?

A: Indeed, some placodes completely failed to develop in the Myh9-dKO mice. However, it is important to emphasize that we defined placode formation by the morphological changes of the epidermal cells and the underlying dermal condensate as well as the compartmentalization of Sox9 expression. As we observed that the pre-placode cell state as defined by FGF20 expression occurs prior to cell shape changes, we have no reason to believe that the early inductive signaling would be defective in these mice.

Q4: Can the experiment where you compress organoids be performed using epidermal progenitor cells from E14.5 Myh9-dKO mice?

A: The isolation of epidermal cells from E14.5 is in principle possible although technically quite a bit more challenging than from E15.5 due to the fragility of the tissue and thus the difficulty to obtain a pure epidermal population.

Q5: Did you observe changes in placodal cell divisions/numbers after blocking MMP activity in dermal fibroblasts? Knowing the complex interplay between MMPs and YAP, would you want to dissect the sequence of their activations?

A: Our data shows that YAP is excluded from the nucleus preceding the switch to budding during which it becomes nuclear and promotes cell cycle re-entry.  This is consistent with previous work from Aurelien Roux and Matthias Lutholf labs showing that compression/confinement exclude nuclear YAP. Thus, we predicted that YAP nuclear re-entry would require release of confinement/compression. One mechanism to achieve this is to remodel the underlying, stiff basement membrane structure, leading us to study the ECM and MMPs which we then show to be important to facilitate the budding. We did not analyse cell divisions but the prediction would be that they would be decreased. The sequence of events observed would further place MMPs upstream of YAP. This would be consistent with work showing the negative correlation between YAP and MMPs. Dissecting this in vivo would indeed be a very interesting new project.

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