Powering morphogenesis: multiscale challenges at the interface of cell adhesion and the cytoskeleton

Fernández-González, Rodrigo; Peifer, Mark

doi:10.1091/mbc.e21-09-0452

Cited by 16 publications

(14 citation statements)

References 143 publications

(161 reference statements)

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“…Our data suggest that AFD-1 localization at junctions in C. elegans depends on HMR-1/cadherin but not HMP-1/α-catenin or SAX-7/L1CAM, which is surprising given previous literature in other systems that suggests an interaction between afadin and α-catenin (34,35). It is possible that multivalent interactions between multiple junctional proteins (62,63) contribute to recruiting AFD-1 to junctions. While afadin is required for proper gastrulation and coordination of junctions with actomyosin contractions, its protein expression is not restricted to only the apically constricting cells.…”

Section: Discussioncontrasting

confidence: 54%

Zyxin contributes to coupling between cell junctions and contractile actomyosin networks during apical constriction

Slabodnick

Tintori

Prakash

et al. 2022

Preprint

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One of the most common cell shape changes driving morphogenesis in diverse animals is the constriction of the apical cell surface. Apical constriction depends on contraction of an actomyosin network in the apical cell cortex, but such actomyosin networks have been shown to undergo continual, conveyor belt-like contractions even before the shrinking of an apical surface begins. This finding suggests that apical constriction is not necessarily triggered by the contraction of actomyosin networks, but rather by unidentified, temporally-regulated mechanical links between actomyosin and junctions. Here, we used C. elegans gastrulation as a model to identify proteins that contribute to such linkage. We found that α-catenin and β-catenin initially failed to move centripetally with contracting cortical actomyosin networks, suggesting that linkage is regulated between cadherin-catenin complexes and actomyosin. We used a proteomic approach to identify AFD-1/afadin and transcriptomics to identify ZYX-1/zyxin as contributors to C. elegans gastrulation. We found that a zyxin family of LIM domain proteins have transcripts that become enriched in multiple cells just before they undergo apical constriction. Using a new, semi-automated image analysis tool, we found that AFD-1/afadin and ZYX-1/zyxin both contribute to cell-cell junctions’ centripetal movement in concert with contracting actomyosin networks. These results identify two key proteins as important for actomyosin networks to effectively pull cell-cell junctions inward during apical constriction. The transcriptional upregulation of zyxin/ZYX-1 in specific cells points to one way that developmental patterning spatiotemporally regulates cell biological mechanisms in vivo. Because afadin- and zyxin-family proteins contribute to membrane-cytoskeleton linkage in other systems, we anticipate that their roles in regulating apical constriction in this manner may be conserved.

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Section: Discussioncontrasting

confidence: 54%

Zyxin contributes to coupling between cell junctions and contractile actomyosin networks during apical constriction

Slabodnick

Tintori

Prakash

et al. 2022

Preprint

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“…Moreover, the trajectory analysis of spatial transcriptomic data enabled us to observe the selective activation of some genes at the early stages of pseudotime, confirming the progenitor nature of this subpopulation. In addition, the microenviroment of this cluster is rich in adherens junctions and vascular cells, which are essential in cell-cell communication, cell renewal and differentiation 48,49 . All these findings suggest that these ID1 + cells might represent a new progenitor population in the adult adrenal cortex.…”

Section: Discussionmentioning

confidence: 99%

Cell Atlas at Single-Nuclei Resolution of the Adult Human Adrenal Gland and Adrenocortical Adenomas

Altieri

Secener

Sai

et al. 2022

Preprint

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The human adrenal gland is a complex endocrine tissue. Developmental studies on this tissue have been limited to animal models or human foetus. Here, we present a cell atlas analysis of the adult human normal adrenal gland, combining single-nuclei RNA sequencing and spatial transcriptome data to reconstruct adrenal gland development and tumourigenesis. We identified two populations of potential progenitor cells resident within the adrenal cortex: adrenocortical progenitors NR2F2+-ID1+ cells, located within and underneath the capsule, and medullary progenitors SYT1+-CHGA- cells, located in islets in the subcapsular region. Using pseudotime analyses, we provided evidence of the centripetal nature of adrenocortical cell development and of the essential role played by the Wnt/β-catenin pathway in the adrenocortical self-renewal. By comparing transcriptional profiles of cells of normal adrenal glands and adrenocortical adenomas we revealed a high heterogeneity with six adenoma-specific clusters. Overall, our results give insights into adrenal plasticity and mechanisms underlying adrenocortical tumourigenesis.

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“…The functions of RhoGTPases have been extensively and systematically investigated in individual cells. However, multicellularity entails a complex interplay between the cytoskeleton and cell-cell junctions to regulate cell and tissue architecture and dynamics (Buckley and St Johnston, 2022; Fernandez-Gonzalez and Peifer, 2022); thus highlighting the relevance of characterizing RhoGEF/GAP function in tissues. Cell division has emerged as a multicellular process, since it entails the deformation of the neighbouring cells, the remodelling of the dividing and neighbour cell junctions, as well as de novo junction formation (Herszterg et al, 2014; Ragkousi and Gibson, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…Building on our findings on Cysts and the ones on p114RhoGEF in vitro (Acharya et al, 2018), one could hypothesize that Cysts/p114RhoGEF represents a common platform for the response to mechanical force during cytokinesis; thus calling for the investigation of the function of RhoGTPases in cells neighbouring the dividing cells in vertebrates. Last, Cysts is involved in AJ integrity, cell-cell rearrangements and cell ingression in interphasic cells in the early Drosophila embryo (Garcia De Las Bayonas et al, 2019; Silver et al, 2019; Simões et al, 2022); processes entailing the production of mechanical forces and the remodelling of the actomyosin cytoskeleton (Fernandez-Gonzalez and Peifer, 2022; Lecuit and Yap, 2015; Pinheiro and Bellaïche, 2018). One could envision that cytoskeleton and junction dynamics might also depend on the Cysts mechanosensing activity in these developmental processes.…”

Section: Discussionmentioning

confidence: 99%

Systematic characterization ofDrosophilaRhoGEF/GAP localizations uncovers regulators of mechanosensing and junction formation during epithelial cell division

Pietro

Osswald

Heras

et al. 2022

Preprint

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Cell proliferation is central to epithelial tissue development, repair and homeostasis. During cell division, small RhoGTPases control both actomyosin dynamics and cell-cell junction remodelling to faithfully segregate the duplicated genome while maintaining tissue polarity and integrity. To decipher the mechanisms of RhoGTPases spatiotemporal regulation during epithelial cell division, we generated a transgenic fluorescently tagged library for Drosophila Rho Guanine exchange factors (GEF) and GTPase activating proteins (GAP), and systematically characterized their endogenous distributions by time-lapse microscopy. Thereby, we unveiled candidate regulators of the interplay between actomyosin and junctional dynamics during epithelial cell division. Building on these findings, we uncovered that during cytokinesis, Cysts and RhoGEF4 play sequential roles in mechanosensing and de novo junction formation, respectively. We foresee that the RhoGEF/GAP library will be a key resource to understand the broad range of biological processes regulated by RhoGTPases.

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Powering morphogenesis: multiscale challenges at the interface of cell adhesion and the cytoskeleton

Cited by 16 publications

References 143 publications

Zyxin contributes to coupling between cell junctions and contractile actomyosin networks during apical constriction

Zyxin contributes to coupling between cell junctions and contractile actomyosin networks during apical constriction

Cell Atlas at Single-Nuclei Resolution of the Adult Human Adrenal Gland and Adrenocortical Adenomas

Systematic characterization ofDrosophilaRhoGEF/GAP localizations uncovers regulators of mechanosensing and junction formation during epithelial cell division

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