scholarly journals Mechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation

2019 ◽  
Author(s):  
Michael C. Holcomb ◽  
Guo-Jie Jason Gao ◽  
Mahsa Servati ◽  
Dylan Schneider ◽  
Presley K. McNeely ◽  
...  
Keyword(s):  
Tensile Stress ◽  
Initial Phase ◽  
Fluid Model ◽  
Drosophila Embryo ◽  
Ventral Region ◽  
Apical Constriction ◽  
Cell Contractility ◽  
Ventral Furrow ◽  
Granular Fluid ◽  
Coupled Stress

AbstractFormation of the ventral furrow in the Drosophila embryo relies on the apical constriction of cells in the ventral region to produce bending forces that drive tissue invagination. Recently [J Phys Condens Matter. 2016;28(41):414021], we observed that apical constrictions during the initial phase of ventral furrow formation produce elongated patterns of cellular constriction chains prior to invagination, and argued that these are indicative of tensile stress feedback. Here, we quantitatively analyze the constriction patterns preceding ventral furrow formation and find that they are consistent with the predictions of our active-granular-fluid model of a monolayer of mechanically coupled stress-sensitive constricting particles. Our model shows that tensile feedback causes constriction chains to develop along underlying precursor tensile stress chains that gradually strengthen with subsequent cellular constrictions. As seen in both our model and available optogenetic experiments, this mechanism allows constriction chains to penetrate or circumvent zones of reduced cell contractility, thus increasing the robustness of ventral furrow formation to spatial variation of cell contractility by rescuing cellular constrictions in the disrupted regions.

scholarly journals Mechanical feedback and robustness of apical constrictions in Drosophila embryo ventral furrow formation

2021 ◽  
Vol 17 (7) ◽  
pp. e1009173
Author(s):  
Michael C. Holcomb ◽  
Guo-Jie Jason Gao ◽  
Mahsa Servati ◽  
Dylan Schneider ◽  
Presley K. McNeely ◽  
...  
Keyword(s):  
Tensile Stress ◽  
Initial Phase ◽  
Fluid Model ◽  
Drosophila Embryo ◽  
Ventral Region ◽  
Apical Constriction ◽  
Cell Contractility ◽  
Ventral Furrow ◽  
Granular Fluid ◽  
Coupled Stress

Formation of the ventral furrow in the Drosophila embryo relies on the apical constriction of cells in the ventral region to produce bending forces that drive tissue invagination. In our recent paper we observed that apical constrictions during the initial phase of ventral furrow formation produce elongated patterns of cellular constriction chains prior to invagination and argued that these are indicative of tensile stress feedback. Here, we quantitatively analyze the constriction patterns preceding ventral furrow formation and find that they are consistent with the predictions of our active-granular-fluid model of a monolayer of mechanically coupled stress-sensitive constricting particles. Our model shows that tensile feedback causes constriction chains to develop along underlying precursor tensile stress chains that gradually strengthen with subsequent cellular constrictions. As seen in both our model and available optogenetic experiments, this mechanism allows constriction chains to penetrate or circumvent zones of reduced cell contractility, thus increasing the robustness of ventral furrow formation to spatial variation of cell contractility by rescuing cellular constrictions in the disrupted regions.

Gastrulation in Drosophila: the formation of the ventral furrow and posterior midgut invaginations

Development ◽  
1991 ◽  
Vol 112 (3) ◽  
pp. 775-789 ◽  
Author(s):  
D. Sweeton ◽  
S. Parks ◽  
M. Costa ◽  
E. Wieschaus
Keyword(s):  
Cell Shape ◽  
Time Course ◽  
Drosophila Embryo ◽  
Second Phase ◽  
Rapid Phase ◽  
Apical Constriction ◽  
Posterior Midgut ◽  
Ventral Furrow ◽  
Two Phases ◽  
Shape Changes

The ventral furrow and posterior midgut invaginations bring mesodermal and endodermal precursor cells into the interior of the Drosophila embryo during gastrulation. Both invaginations proceed through a similar sequence of rapid cell shape changes, which include apical flattening, constriction of the apical diameter, cell elongation and subsequent shortening. Based on the time course of apical constriction in the ventral furrow and posterior midgut, we identify two phases in this process: first, a slow stochastic phase in which some individual cells begin to constrict and, second, a rapid phase in which the remaining unconstricted cells constrict. Mutations in the concertina or folded gastrulation genes appear to block the transition to the second phase in both the ventral furrow and the posterior midgut invaginations.

scholarly journals Novel patterns of homeotic protein accumulation in the head of the Drosophila embryo

Development ◽  
1989 ◽  
Vol 105 (1) ◽  
pp. 167-174 ◽  
Author(s):  
J.W. Mahaffey ◽  
R.J. Diederich ◽  
T.C. Kaufman
Keyword(s):  
Nerve Cord ◽  
Protein Product ◽  
Drosophila Embryo ◽  
Protein Accumulation ◽  
Homeotic Genes ◽  
Gene Products ◽  
Ventral Region ◽  
Sex Combs Reduced ◽  
Sex Combs ◽  
Dorsal Epidermis

Antibodies that specifically recognize proteins encoded by the homeotic genes: Sex combs reduced, Deformed, labial and proboscipedia, were used to follow the distribution of these gene products during embryogenesis. The position of engrailed-expressing cells was used as a reference and staining conditions were established that could distinguish, among cells expressing engrailed, one of the homeotic proteins or both. Our observations demonstrate two important facts about establishing identity in the head segments. First, in contrast to the overlapping pattern of homeotic gene expression in the trunk segments, we observe a non-overlapping pattern in the head for those homeotic proteins required during embryogenesis. In contrast, the spatial accumulation of the protein product of the non-vital proboscipedia locus overlaps partially with the distribution of the Deformed and Sex combs reduced proteins in the maxillary and labial segments, respectively. Second, two of the proteins, Sex combs reduced and Deformed, have different dorsal and ventral patterns of accumulation. Dorsally, these proteins are expressed in segmental domains while, within the ventral region, a parasegmental register is observed. The boundary where this change in pattern occurs coincides with the junction between the ventral neurogenic region and the dorsal epidermis. After contraction of the germ band, when the nerve cord has completely separated from the epidermis, the parasegmental pattern is observed only within the ventral nerve cord while a segmental register is maintained throughout the epidermis.

scholarly journals DRhoGEF2 and Diaphanous Regulate Contractile Force during Segmental Groove Morphogenesis in the Drosophila Embryo

2008 ◽  
Vol 19 (5) ◽  
pp. 1883-1892 ◽  
Author(s):  
Shai Mulinari ◽  
Mojgan Padash Barmchi ◽  
Udo Häcker
Keyword(s):  
Cell Shape ◽  
Cell Formation ◽  
Small Gtpases ◽  
Cell Junctions ◽  
Drosophila Embryo ◽  
Cell Cortex ◽  
Nucleotide Exchange ◽  
Apical Constriction ◽  
Guanine Nucleotide Exchange ◽  
Nucleotide Exchange Factors

Morphogenesis of the Drosophila embryo is associated with dynamic rearrangement of the actin cytoskeleton mediated by small GTPases of the Rho family. These GTPases act as molecular switches that are activated by guanine nucleotide exchange factors. One of these factors, DRhoGEF2, plays an important role in the constriction of actin filaments during pole cell formation, blastoderm cellularization, and invagination of the germ layers. Here, we show that DRhoGEF2 is equally important during morphogenesis of segmental grooves, which become apparent as tissue infoldings during mid-embryogenesis. Examination of DRhoGEF2-mutant embryos indicates a role for DRhoGEF2 in the control of cell shape changes during segmental groove morphogenesis. Overexpression of DRhoGEF2 in the ectoderm recruits myosin II to the cell cortex and induces cell contraction. At groove regression, DRhoGEF2 is enriched in cells posterior to the groove that undergo apical constriction, indicating that groove regression is an active process. We further show that the Formin Diaphanous is required for groove formation and strengthens cell junctions in the epidermis. Morphological analysis suggests that Dia regulates cell shape in a way distinct from DRhoGEF2. We propose that DRhoGEF2 acts through Rho1 to regulate acto-myosin constriction but not Diaphanous-mediated F-actin nucleation during segmental groove morphogenesis.

scholarly journals RhoA GTPase inhibition organizes contraction during epithelial morphogenesis

2016 ◽  
Vol 214 (5) ◽  
pp. 603-617 ◽  
Author(s):  
Frank M. Mason ◽  
Shicong Xie ◽  
Claudia G. Vasquez ◽  
Michael Tworoger ◽  
Adam C. Martin
Keyword(s):  
Cell Shape ◽  
Shape Change ◽  
Critical Role ◽  
Central Position ◽  
Nucleotide Exchange ◽  
Apical Constriction ◽  
Cell Contractility ◽  
Rhoa Activity ◽  
Cell Shape Change ◽  
Rhoa Gtpase

During morphogenesis, contraction of the actomyosin cytoskeleton within individual cells drives cell shape changes that fold tissues. Coordination of cytoskeletal contractility is mediated by regulating RhoA GTPase activity. Guanine nucleotide exchange factors (GEFs) activate and GTPase-activating proteins (GAPs) inhibit RhoA activity. Most studies of tissue folding, including apical constriction, have focused on how RhoA is activated by GEFs to promote cell contractility, with little investigation as to how GAPs may be important. Here, we identify a critical role for a RhoA GAP, Cumberland GAP (C-GAP), which coordinates with a RhoA GEF, RhoGEF2, to organize spatiotemporal contractility during Drosophila melanogaster apical constriction. C-GAP spatially restricts RhoA pathway activity to a central position in the apical cortex. RhoGEF2 pulses precede myosin, and C-GAP is required for pulsation, suggesting that contractile pulses result from RhoA activity cycling. Finally, C-GAP expression level influences the transition from reversible to irreversible cell shape change, which defines the onset of tissue shape change. Our data demonstrate that RhoA activity cycling and modulating the ratio of RhoGEF2 to C-GAP are required for tissue folding.

scholarly journals Functional plasticity of polarity proteins controls epithelial tissue architecture

2021 ◽  
Author(s):  
Cornélia Biehler ◽  
Katheryn E. Rothenberg ◽  
Alexandra Jetté ◽  
Hélori-Mael Gaudé ◽  
Rodrigo Fernandez-Gonzalez ◽  
...  
Keyword(s):  
Epithelial Cells ◽  
Domain Size ◽  
Cell Polarization ◽  
Epithelial Tissue ◽  
Tissue Architecture ◽  
Functional Plasticity ◽  
Apical Constriction ◽  
Dynamic Regulation ◽  
Cell Contractility ◽  
Apical Domain

AbstractThe Drosophila polarity protein Crumbs is essential for the establishment and growth of the apical domain in epithelial cells. Dynamic regulation of apical domain size is crucial for forming and maintaining complex epithelial structures such as tubes or acini. The protein Yurt limits the ability of Crumbs to promote apical membrane growth, thereby defining proper apical/basal membrane ratio that is essential for the functional architecture of epithelial cells. Here, we show that Yurt is not a general inhibitor of Crumbs, but rather hijacks Crumbs activity toward specific functions. In particular, Crumbs recruits Yurt to the apical domain to increase Myosin-dependent cortical tension while decreasing relative tissue viscosity. Yurt overexpression thus induces apical constriction in epithelial cells. The kinase aPKC phosphorylates Yurt, thereby dislodging the latter from the apical domain and releasing apical tension. In contrast, the kinase Pak1 promotes Yurt dephosphorylation through activation of the phosphatase PP2A. The Pak1–PP2A module thus opposes aPKC function and supports Yurt-induced apical constriction. Hence, the complex interplay between Yurt, aPKC, Pak1 and PP2A contributes to the functional plasticity of Crumbs. Overall, our data increase our understanding of how proteins sustaining epithelial cell polarization and Myosin-dependent cell contractility interact with one another to control epithelial tissue architecture.

scholarly journals Morphogenetic forces planar polarize LGN/Pins in the embryonic head during Drosophila gastrulation

2022 ◽  
Author(s):  
Jaclyn M Camuglia ◽  
Soline Chanet ◽  
Adam C Martin
Keyword(s):  
Planar Cell Polarity ◽  
Adherens Junction ◽  
Drosophila Embryo ◽  
Spindle Orientation ◽  
Planar Polarity ◽  
Ventral Furrow ◽  
Adherens Junction Protein ◽  
Early Drosophila Embryo ◽  
Junction Protein

Spindle orientation is often achieved by a complex of Pins/LGN, Mud/NuMa, Gαi, and Dynein, which interacts with astral microtubules to rotate the spindle. Cortical Pins/LGN recruitment serves as a critical step in this process. Here, we identify Pins-mediated planar cell polarized divisions in several of the mitotic domains of the early Drosophila embryo. We found that neither planar cell polarity pathways nor planar polarized myosin localization determined division orientation; instead, our findings strongly suggest that Pins planar polarity and force generated from mesoderm invagination are important. Disrupting Pins polarity via overexpression of a myristoylated version of Pins caused randomized division angles. We found that disrupting forces through chemical inhibitors, laser ablation, and depletion of an adherens junction protein disrupted Pins planar polarity and spindle orientation. Furthermore, snail depletion, which abrogates ventral furrow forces, disrupted Pins polarization and spindle orientation, suggesting that morphogenetic movements and resulting forces transmitted through the tissue can polarize Pins and orient division. Thus, morphogenetic forces associated with mesoderm invagination result in planar polarized Pins to mediate division orientation at a distant region of the embryo during morphogenesis. To our knowledge, this is the first in vivo example where mechanical force has been shown to polarize Pins to mediate division orientation.

scholarly journals Loss of Gα12/13 exacerbates apical area dependence of actomyosin contractility

2016 ◽  
Vol 27 (22) ◽  
pp. 3526-3536 ◽  
Author(s):  
Shicong Xie ◽  
Frank M. Mason ◽  
Adam C. Martin
Keyword(s):  
Cell Shape ◽  
Rho Kinase ◽  
Dependent Manner ◽  
Timely Initiation ◽  
Apical Constriction ◽  
Size Dependent ◽  
Actin Cortex ◽  
Ventral Furrow ◽  
Delayed Initiation ◽  
Apical Area

During development, coordinated cell shape changes alter tissue shape. In the Drosophila ventral furrow and other epithelia, apical constriction of hundreds of epithelial cells folds the tissue. Genes in the Gα12/13 pathway coordinate collective apical constriction, but the mechanism of coordination is poorly understood. Coupling live-cell imaging with a computational approach to identify contractile events, we discovered that differences in constriction behavior are biased by initial cell shape. Disrupting Gα12/13 exacerbates this relationship. Larger apical area is associated with delayed initiation of contractile pulses, lower apical E-cadherin and F-actin levels, and aberrantly mobile Rho-kinase structures. Our results suggest that loss of Gα12/13 disrupts apical actin cortex organization and pulse initiation in a size-dependent manner. We propose that Gα12/13 robustly organizes the apical cortex despite variation in apical area to ensure the timely initiation of contractile pulses in a tissue with heterogeneity in starting cell shape.

Sign in / Sign up

Export Citation Format

Share Document