Complete canthi removal reveals that forces from the amnioserosa alone are sufficient to drive dorsal closure in<i>Drosophila</i>

Wells, Adrienne R.; Zou, Roger S.; Tulu, U. Serdar; Sokolow, Adam; Crawford, Jennifer L.; Edwards, Glenn S.; Kiehart, Daniel P.

doi:10.1091/mbc.e14-07-1190

Cited by 42 publications

(60 citation statements)

References 44 publications

(104 reference statements)

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“…S2), arguing against inefficient closure as the basis for the late defects. The velocity of the LEs, defined as dH/dt averaged over the duration of closure, was 14±4 and 13±4 nm/s for Pvr heterozygous and homozygous mutant embryos, respectively, similar to published velocities (Hutson et al, 2003;Wells et al, 2014). Time-lapse imaging did however suggest faltering of zipping in some embryos, which was appreciated by projecting time series data as 2D images (Fig.…”

Section: Pvr Protein Expression In the As And Ectodermsupporting

confidence: 65%

Pvr receptor tyrosine kinase promotes tissue closure by coordinating corpse removal and epidermal zippering

et al. 2015

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A leading cause of human birth defects is the incomplete fusion of tissues, often manifested in the palate, heart, or neural tube. To investigate the molecular control of tissue fusion, embryonic dorsal closure and pupal thorax closure in Drosophila are useful experimental models. We find that Pvr mutants have defects in dorsal midline closure with incomplete amnioserosa internalization and epidermal zippering, as well as cardia bifida. These defects are relatively mild in comparison to those seen with other signaling mutants such as the JNK pathway, and we demonstrate that JNK signaling is not perturbed by altering Pvr receptor tyrosine kinase activity. Rather, modulation of Pvr levels in the ectoderm has an impact on PIP3 membrane accumulation consistent with a link to PI3K signal transduction. Polarized PI3K activity influences protrusive activity from the epidermal leading edge and protrusion area changes in accord with Pvr signaling intensity, providing a possible mechanism to explain Pvr mutant phenotypes. Tissue specific rescue experiments indicate a partial requirement in epithelial tissue, but confirm the essential role of Pvr in the hemocytes for embryonic survival. Taken together, we argue that inefficient removal of the internalizing amnioserosa tissue by mutant hemocytes coupled with impaired midline zippering of mutant epithelium creates a situation in some embryos where dorsal midline closure is incomplete. Based on these observations, we suggest that efferocytosis (corpse clearance) could contribute to proper tissue closure and thus may underlie some congenital birth defects.

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Section: Pvr Protein Expression In the As And Ectodermsupporting

confidence: 65%

Pvr receptor tyrosine kinase promotes tissue closure by coordinating corpse removal and epidermal zippering

et al. 2015

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“…Without these forces, one or both morphogenetic processes fail. This final step is supported by previous experiments in which germband retraction and/or dorsal closure failed because amnioserosa structural integrity was disrupted by either laser ablation (Kiehart et al, ; Hutson et al, ; Toyama et al, ; Solon et al, ; Lynch et al, ; Wells et al, ) or widespread premature apoptosis (U‐shaped group mutants; Frank and Rushlow, ; GoldmanLevi et al, ; Lamka and Lipshitz, ).…”

Section: Discussionsupporting

confidence: 58%

“…For the latter two phenotypes, 17 of 19 embryos displaying one of the two defects also had holes at the earlier observation timepoint. Correlation is of course not causation, but previous work on the mechanics of both germband retraction and dorsal closure showed that the amnioserosa makes a critically important contribution to the forces driving those processes (Hutson et al, 2003;Toyama et al, 2008;Solon et al, 2009;Lynch et al, 2013Lynch et al, , 2014Wells et al, 2014). These processes can fail if the amnioserosa's structural integrity is compromised by means of laser ablation (Hutson et al, 2003;Lynch et al, 2013) or mutations (Frank and Rushlow, 1996;Reed et al, 2004); heat-shock-induced holes could do the same.…”

Section: Do Amnioserosa Holes Cause Subsequent Development Defects?mentioning

confidence: 99%

Pathway to a phenocopy: Heat stress effects in early embryogenesis

Crews

McCleery

Hutson

2015

Developmental Dynamics

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Background Heat shocks applied at the onset of gastrulation in early Drosophila embryos frequently lead to phenocopies of U-shaped mutants – having characteristic failures in the late morphogenetic processes of germband retraction and dorsal closure. The pathway from non-specific heat stress to phenocopied abnormalities is unknown. Results Drosophila embryos subjected to 30-min, 38-°C heat shocks at gastrulation appear to recover and restart morphogenesis. Post-heat-shock development appears normal, albeit slower, until a large fraction of embryos develop amnioserosa holes (diameters > 100 μm). These holes are positively correlated with terminal U-shaped phenocopies. They initiate between amnioserosa cells and open over tens of minutes by evading normal wound healing responses. They are not caused by tissue-wide increases in mechanical stress or decreases in cell-cell adhesion, but instead appear to initiate from isolated apoptosis of amnioserosa cells. Conclusions The pathway from heat shock to U-shaped phenocopies involves the opening of one or more large holes in the amnioserosa that compromise its structural integrity and lead to failures in morphogenetic processes that rely on amnioserosa-generated tensile forces. The proposed mechanism by which heat shock leads to hole initiation and expansion is heterochonicity – i.e., disruption of morphogenetic coordination between embryonic and extra-embryonic cell types.

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“…However, several lines of evidence suggest that a ratchet mechanism stabilising the contracted state of amnioserosa cells is acting at the level of individual cells (Blanchard et al, 2010;Wang et al, 2012;Wells et al, 2014). In particular, the analysis performed here of actin oscillatory dynamics in α-Cat mutants suggests that the increase in the expansion half-cycle of amnioserosa apical cell oscillations could be due to an increase in the time interval between the appearance of consecutive foci.…”

Section: Discussionmentioning

confidence: 73%

α-Catenin stabilises Cadherin–Catenin complexes and modulates actomyosin dynamics to allow pulsatile apical contraction

Jurado

Navascués

Gorfinkiel

2016

Journal of Cell Science

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We have investigated how cell contractility and adhesion are functionally integrated during epithelial morphogenesis. To this end, we have analysed the role of α-Catenin, a key molecule linking E-Cadherin-based adhesion and the actomyosin cytoskeleton, during Drosophila embryonic dorsal closure, by studying a newly developed allelic series. We find that α-Catenin regulates pulsatile apical contraction in the amnioserosa, the main force-generating tissue driving closure of the embryonic epidermis. α-Catenin controls actomyosin dynamics by stabilising and promoting the formation of actomyosin foci, and also stabilises DE-Cadherin (Drosophila E-Cadherin, also known as Shotgun) at the cell membrane, suggesting that medioapical actomyosin contractility regulates junction stability. Furthermore, we uncover a genetic interaction between α-Catenin and Vinculin, and a tension-dependent recruitment of Vinculin to amniosersoa apical cell membranes, suggesting the existence of a mechano-sensitive module operating in this tissue.

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Complete canthi removal reveals that forces from the amnioserosa alone are sufficient to drive dorsal closure inDrosophila

Cited by 42 publications

References 44 publications

Pvr receptor tyrosine kinase promotes tissue closure by coordinating corpse removal and epidermal zippering

Pvr receptor tyrosine kinase promotes tissue closure by coordinating corpse removal and epidermal zippering

Pathway to a phenocopy: Heat stress effects in early embryogenesis

α-Catenin stabilises Cadherin–Catenin complexes and modulates actomyosin dynamics to allow pulsatile apical contraction

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