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

2020 ◽  
Author(s):  
Marlis Denk-Lobnig ◽  
Natalie C Heer ◽  
Adam C Martin
Keyword(s):  
Gene Expression ◽  
Cell Mechanics ◽  
Cell Shape ◽  
Quantitative Imaging ◽  
Expression Patterns ◽  
Rhoa Activation ◽  
Ventral Furrow ◽  
Distinct Cell ◽  
Cell Shape Changes ◽  
Shape Changes

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.

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
Keyword(s):  
Cell Mechanics ◽  
Cell Shape ◽  
Transcriptional Activity ◽  
Quantitative Imaging ◽  
Elastic Shell ◽  
Force Transmission ◽  
Rhoa Activation ◽  
Distinct Cell ◽  
Cell Shape Changes ◽  
Shape Changes

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.

scholarly journals Hyperactivation of the folded gastrulation pathway induces specific cell shape changes

Development ◽  
1998 ◽  
Vol 125 (4) ◽  
pp. 589-597 ◽  
Author(s):  
P. Morize ◽  
A.E. Christiansen ◽  
M. Costa ◽  
S. Parks ◽  
E. Wieschaus
Keyword(s):  
Cell Shape ◽  
Inducible Promoter ◽  
Specific Cell ◽  
Apical Surface ◽  
Apical Constriction ◽  
Cellular Effects ◽  
Ventral Furrow ◽  
Cell Shape Changes ◽  
Shape Changes

During Drosophila gastrulation, mesodermal precursors are brought into the interior of the embryo by formation of the ventral furrow. The first steps of ventral furrow formation involve a flattening of the apical surface of the presumptive mesodermal cells and a constriction of their apical diameters. In embryos mutant for folded gastrulation (fog), these cell shape changes occur but the timing and synchrony of the constrictions are abnormal. A similar phenotype is seen in a maternal effect mutant, concertina (cta). fog encodes a putative secreted protein whereas cta encodes an (alpha)-subunit of a heterotrimeric G protein. We have proposed that localized expression of the fog signaling protein induces apical constriction by interacting with a receptor whose downstream cellular effects are mediated by the cta G(alpha)protein. <P> In order to test this model, we have ectopically expressed fog at the blastoderm stage using an inducible promoter. In addition, we have examined the constitutive activation of cta protein by blocking GTP hydrolysis using both in vitro synthesized mutant alleles and cholera toxin treatment. Activation of the fog/cta pathway by any of these procedures results in ectopic cell shape changes in the gastrula. Uniform fog expression rescues the gastrulation defects of fog null embryos but not cta mutant embryos, arguing that cta functions downstream of fog expression. The normal location of the ventral furrow in embryos with uniformly expressed fog suggests the existence of a fog-independent pathway determining mesoderm-specific cell behaviors and invagination. Epistasis experiments indicate that this pathway requires snail but not twist expression.

Mechanisms of early Drosophila mesoderm formation

Development ◽  
1992 ◽  
Vol 116 (Supplement) ◽  
pp. 23-31 ◽  
Author(s):  
Maria Leptin ◽  
José Casal ◽  
Barbara Grunewald ◽  
Rolf Reuter
Keyword(s):  
Cell Shape ◽  
Cell Populations ◽  
Genetic Screens ◽  
Germ Band ◽  
Posterior Midgut ◽  
Ventral Furrow ◽  
Mesoderm Formation ◽  
Cell Shape Changes ◽  
Shape Changes ◽  
Different Parts

Several morphogenetic processes occur simultaneously during Drosophila gastrulation, including ventral furrow invagination to form the mesoderm, anterior and posterior midgut invagination to create the endoderm, and germ band extension. Mutations changing the behaviour of different parts of the embryo can be used to test the roles of different cell populations in gastrulation. Posterior midgut morphogenesis and germ band extension are partly independent, and neither depends on mesoderm formation, nor mesoderm formation on them. The invagination of the ventral furrow is caused by forces from within the prospective mesoderm (i. e. the invaginating cells) without any necessary contribution from other parts of the embryo. The events that lead to the cell shape changes mediating ventral furrow formation require the transcription of zygotic genes under the control of twist and snail. Such genes can be isolated by molecular and genetic screens.

Regulatory network for cell shape changes during Drosophila ventral furrow formation

2006 ◽  
Vol 239 (1) ◽  
pp. 49-62 ◽  
Author(s):  
Julio Aracena ◽  
Mauricio González ◽  
Alejandro Zuñiga ◽  
Marco A. Mendez ◽  
Verónica Cambiazo
Keyword(s):  
Regulatory Network ◽  
Cell Shape ◽  
Ventral Furrow ◽  
Cell Shape Changes ◽  
Shape Changes

Animal cell shape changes and gene expression

BioEssays ◽  
1991 ◽  
Vol 13 (5) ◽  
pp. 207-212 ◽  
Author(s):  
Avri Ben-Ze've
Keyword(s):  
Gene Expression ◽  
Cell Shape ◽  
Animal Cell ◽  
Cell Shape Changes ◽  
Shape Changes

Drosophila gastrulation: analysis of cell shape changes in living embryos by three-dimensional fluorescence microscopy

Development ◽  
1991 ◽  
Vol 112 (2) ◽  
pp. 365-370 ◽  
Author(s):  
Z. Kam ◽  
J.S. Minden ◽  
D.A. Agard ◽  
J.W. Sedat ◽  
M. Leptin
Keyword(s):  
Cell Shape ◽  
Three Dimensional ◽  
Time Lapse ◽  
Second Phase ◽  
Fluorescent Markers ◽  
Ventral Furrow ◽  
Cell Shapes ◽  
Cell Shape Changes ◽  
Two Phases ◽  
Shape Changes

The first event of Drosophila gastrulation is the formation of the ventral furrow. This process, which leads to the invagination of the mesoderm, is a classical example of epithelial folding. To understand better the cellular changes and dynamics of furrow formation, we examined living Drosophila embryos using three-dimensional time-lapse microscopy. By injecting fluorescent markers that visualize cell outlines and nuclei, we monitored changes in cell shapes and nuclear positions. We find that the ventral furrow invaginates in two phases. During the first ‘preparatory’ phase, many prospective furrow cells in apparently random positions gradually begin to change shape, but the curvature of the epithelium hardly changes. In the second phase, when a critical number of cells have begun to change shape, the furrow suddenly invaginates. Our results suggest that furrow formation does not result from an ordered wave of cell shape changes, contrary to a model for epithelial invagination in which a wave of apical contractions causes invagination. Instead, it appears that cells change their shape independently, in a stochastic manner, and the sum of these individual changes alters the curvature of the whole epithelium.

Cell shape changes during gastrulation in Drosophila

Development ◽  
1990 ◽  
Vol 110 (1) ◽  
pp. 73-84 ◽  
Author(s):  
M. Leptin ◽  
B. Grunewald
Keyword(s):  
Cell Fate ◽  
Cell Shape ◽  
Multilayered Structure ◽  
Second Phase ◽  
Specific Cell ◽  
Ventral Furrow ◽  
Correct Execution ◽  
Cell Shape Changes ◽  
Two Phases ◽  
Shape Changes

The first morphogenetic movement during Drosophila development is the invagination of the mesoderm, an event that folds a one-layered epithelium into a multilayered structure. In this paper, we describe the shape changes and behaviour of the cells participating in this process and show how mutations that change cell fate affect this behaviour. We divide the formation of the mesodermal germ layer into two phases. During the first phase, the ventral epithelium folds into a tube by a series of concerted cell shape changes (ventral furrow formation). Based on the behaviour of cells in this phase, we conclude that the prospective mesoderm is not a homogeneous cell population, but consists of two subpopulations. Each subpopulation goes through a distinctive sequence of specific cell shape changes which together mediate the invagination of the ventral furrow. In the second phase, the invaginated tube of mesoderm loses its epithelial character, the mesoderm cells disperse, divide and then spread out along the ectoderm to form a single cell layer. To test how ventral furrow formation depends on cell fates in the mesoderm and in neighbouring cells we alter these fates genetically using maternal and zygotic mutations. These experiments show that some of the aspects of cell behaviour specific for ventral furrow cells are part of an autonomous differentiation programme. The force driving the invagination is generated within the region of the ventral furrow, with the lateral and dorsal cell populations contributing little or none of the force. Two known zygotic genes that are required for the formation of the mesoderm, twist and snail, are expressed in ventral furrow cells, and the correct execution of cell shape changes in the mesoderm depends on both. Finally, we show that the region where the ventral furrow forms is determined by the expression of mesoderm-specific genes, and not by mechanical or other epigenetic properties of the egg.

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