scholarly journals Combinatorial patterns of graded RhoA activation and uniform F-actin depletion promote tissue curvature

Development ◽  
2021 ◽  
Author(s):  
Marlis Denk-Lobnig ◽  
Jan F Totz ◽  
Natalie C Heer ◽  
Jörn Dunkel ◽  
Adam C Martin

During development, gene expression regulates cell mechanics and shape to sculpt tissues. Epithelial folding proceeds through distinct cell shape changes that occur simultaneously in different regions of a tissue. Here, using quantitative imaging in Drosophila melanogaster, we investigate how patterned cell shape changes promote tissue bending during early embryogenesis. We find that the transcription factors Twist and Snail combinatorially regulate a multicellular pattern of lateral F-actin density that differs from the previously described myosin-2 gradient. This F-actin pattern correlates with whether cells apically constrict, stretch, or maintain their shape. We show that the myosin-2 gradient and F-actin depletion do not depend on force transmission, suggesting that transcriptional activity is required to create these patterns. The myosin-2 gradient width results from a gradient in RhoA activation that is refined through the balance between RhoGEF2 and the RhoGAP C-GAP. Our experimental results and simulations of a 3D elastic shell model show that tuning gradient width regulates tissue curvature.

Author(s):  
Marlis Denk-Lobnig ◽  
Natalie C Heer ◽  
Adam C Martin

AbstractDuring development, gene expression regulates cell mechanics and shape to sculpt tissues. Epithelial folding proceeds through distinct cell shape changes that occur in different regions of a tissue. Here, using quantitative imaging in Drosophila melanogaster, we investigate how patterned cell shape changes promote tissue bending during early embryogenesis. We find that the transcription factors Twist and Snail combinatorially regulate a unique multicellular pattern of junctional F-actin density, which corresponds to whether cells apically constrict, stretch, or maintain their shape. Part of this pattern is a gradient in junctional F-actin and apical myosin-2, and the width of this gradient regulates tissue curvature. The actomyosin gradient results from a gradient in RhoA activation that is refined by a balance between RhoGEF2 and the RhoGAP C-GAP. Thus, cell behavior in the ventral furrow is choreographed by the interplay of distinct gene expression patterns and this coordination regulates tissue shape.


2021 ◽  
Vol 11 (4) ◽  
Author(s):  
Molly C Jud ◽  
Josh Lowry ◽  
Thalia Padilla ◽  
Erin Clifford ◽  
Yuqi Yang ◽  
...  

AbstractMorphogenesis involves coordinated cell migrations and cell shape changes that generate tissues and organs, and organize the body plan. Cell adhesion and the cytoskeleton are important for executing morphogenesis, but their regulation remains poorly understood. As genes required for embryonic morphogenesis may have earlier roles in development, temperature-sensitive embryonic-lethal mutations are useful tools for investigating this process. From a collection of ∼200 such Caenorhabditis elegans mutants, we have identified 17 that have highly penetrant embryonic morphogenesis defects after upshifts from the permissive to the restrictive temperature, just prior to the cell shape changes that mediate elongation of the ovoid embryo into a vermiform larva. Using whole genome sequencing, we identified the causal mutations in seven affected genes. These include three genes that have roles in producing the extracellular matrix, which is known to affect the morphogenesis of epithelial tissues in multicellular organisms: the rib-1 and rib-2 genes encode glycosyltransferases, and the emb-9 gene encodes a collagen subunit. We also used live imaging to characterize epidermal cell shape dynamics in one mutant, or1219ts, and observed cell elongation defects during dorsal intercalation and ventral enclosure that may be responsible for the body elongation defects. These results indicate that our screen has identified factors that influence morphogenesis and provides a platform for advancing our understanding of this fundamental biological process.


Glia ◽  
1992 ◽  
Vol 6 (3) ◽  
pp. 180-187 ◽  
Author(s):  
Ignacio Torres-Aleman ◽  
Maria Teresa Rejas ◽  
Sebastian Pons ◽  
Luis Miguel Garcia-Segura

Open Biology ◽  
2018 ◽  
Vol 8 (11) ◽  
pp. 180124 ◽  
Author(s):  
Jack Daniel Sunter ◽  
Flavia Moreira-Leite ◽  
Keith Gull

Flagella have multiple functions that are associated with different axonemal structures. Motile flagella typically have a 9 + 2 arrangement of microtubules, whereas sensory flagella normally have a 9 + 0 arrangement. Leishmania exhibits both of these flagellum forms and differentiation between these two flagellum forms is associated with cytoskeletal and cell shape changes. We disrupted flagellum elongation in Leishmania by deleting the intraflagellar transport (IFT) protein IFT140 and examined the effects on cell morphogenesis. Δift140 cells have no external flagellum, having only a very short flagellum within the flagellar pocket. This short flagellum had a collapsed 9 + 0 (9v) axoneme configuration reminiscent of that in the amastigote and was not attached to the pocket membrane. Although amastigote-like changes occurred in the flagellar cytoskeleton, the cytoskeletal structures of Δift140 cells retained their promastigote configurations, as examined by fluorescence microscopy of tagged proteins and serial electron tomography. Thus, Leishmania promastigote cell morphogenesis does not depend on the formation of a long flagellum attached at the neck. Furthermore, our data show that disruption of the IFT system is sufficient to produce a switch from the 9 + 2 to the collapsed 9 + 0 (9v) axonemal structure, echoing the process that occurs during the promastigote to amastigote differentiation.


2018 ◽  
Vol 115 (11) ◽  
pp. 2259-2270
Author(s):  
Gonca Erdemci-Tandogan ◽  
Madeline J. Clark ◽  
Jeffrey D. Amack ◽  
M. Lisa Manning

2017 ◽  
Author(s):  
Ghislain Gillard ◽  
Ophélie Nicolle ◽  
Thibault Brugières ◽  
Sylvain Prigent ◽  
Mathieu Pinot ◽  
...  

AbstractTissues from different developmental origins must interact to achieve coordinated morphogenesis at the level of a whole organism. C. elegans embryonic elongation is controlled by actomyosin dynamics which trigger cell shape changes in the epidermis and by muscle contractions, but how the two processes are coordinated is not known. We found that a tissue-wide tension generated by muscle contractions and relayed by tendon-like hemidesmosomes in the dorso-ventral epidermis is required to establish a planar polarity of the apical PAR module in the lateral epidermis. This planar polarized PAR module then controls actin planar organization, thus determining the orientation of cell shape changes and the elongation axis of the whole embryo. This trans-tissular mechanotransduction pathway thus contributes to coordinate the morphogenesis of three embryonic tissues.


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