Localization and requirement for Myosin II at the dorsal‐ventral compartment boundary of the <i>Drosophila</i> wing

Major, Robert J.; Irvine, Kenneth D.

doi:10.1002/dvdy.20966

Cited by 124 publications

(149 citation statements)

References 44 publications

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“…S7). Polarized enrichment of MyoII in cells abutting the compartment boundaries, leading to changes in cell shape, have been reported (Landsberg et al, 2009;Major and Irvine, 2006). Our results show that these singular mechanical properties at the compartment boundaries are also present in the bulk of the tissue.…”

Section: Research Articlesupporting

confidence: 72%

A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc

2013

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Organismal development is under genetic control. Ultimately, mechanical forces shape embryos. If we want to understand the precise regulation of size and shape in animals, we must dissect how forces are distributed in developing tissues, and how they drive cell behavior to shape organs. This has not been addressed fully in the context of growing tissues. As cells grow and divide, they exert a pressure on their neighbors. How these local stresses add up or dissipate as the tissue grows is an unanswered question. We address this issue in the growing wing imaginal disc of Drosophila larvae, the precursor of the adult wing. We used a quantitative approach to analyze the strains and stresses of cells of the wing pouch, and found a global pattern of stress whereby cells in the periphery of the tissue are mechanically stretched and cells in the center are compressed. This pattern has important consequences on cell shape in the wing pouch: cells respond to it by polarizing their acto-myosin cortex, and aligning their divisions with the main axis of cell stretch, thereby polarizing tissue growth. Ectopic perturbations of tissue growth by the Hippo signaling pathway reorganize this pattern in a non-autonomous manner, suggesting a synergy between tissue mechanics and growth control during wing disc morphogenesis.

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Section: Research Articlesupporting

confidence: 72%

A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc

2013

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“…6D). Similar cells expressing higher levels of Sqh have been found at the DV compartment boundary of wing discs and are thought to act as a fence between dorsal and ventral cells (Major and Irvine, 2006). The LECs at the segmental borders in the abdomen might also act as a fence, canalising the moving cell mass and restraining its lateral expansion.…”

Section: Some Lecs Appear To Canalise the Dorsal Migration Of The Hismentioning

confidence: 65%

Cell rearrangements, cell divisions and cell death in a migrating epithelial sheet in the abdomen ofDrosophila

Bischoff

Cseresnyés

2009

Development

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During morphogenesis, cell movements, cell divisions and cell death work together to form complex patterns and to shape organs. These events are the outcome of decisions made by many individual cells, but how these decisions are controlled and coordinated is elusive. The adult abdominal epidermis of Drosophila is formed during metamorphosis by divisions and extensive cell migrations of the diploid histoblasts, which replace the polyploid larval cells. Using in vivo 4D microscopy, we have studied the behaviour of the histoblasts and analysed in detail how they reach their final position and to what extent they rearrange during their spreading. Tracking individual cells, we show that the cells migrate in two phases that differ in speed, direction and amount of cellular rearrangement. Cells of the anterior (A) and posterior (P) compartments differ in their behaviour. Cells near the A/P border are more likely to change their neighbours during migration. The mitoses do not show any preferential orientation. After mitosis, the sisters become preferentially aligned with the direction of movement. Thus, in the abdomen, it is the extensive cell migrations that appear to contribute most to morphogenesis. This contrasts with other developing epithelia, such as the wing imaginal disc and the embryonic germband in Drosophila, where oriented mitoses and local cell rearrangements appear to direct morphogenesis. Furthermore, our results suggest that an active force created by the histoblasts contributes to the formation of the adult epidermis. Finally, we show that histoblasts occasionally undergo apoptosis.

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“…Simulations of tissue growth with two compartments furthermore suggest that such local increases in cell bond tension can prevent cell mixing between two adjacent cell populations and can account for the straight shape of compartment boundaries (Landsberg et al, 2009;Aliee et al, 2012). Consistent with these data, reducing Myosin II activity, either throughout the tissue or locally along the compartment boundary, compromises boundary shape (Major and Irvine, 2006;Landsberg et al, 2009;Monier et al, 2010;Aliee et al, 2012;Calzolari et al, 2014). Recent data suggest that local increases in cell bond tension bias cell rearrangements to maintain the straight shape of compartment boundaries (Umetsu et al, 2014).…”

Section: Introductionmentioning

confidence: 71%

A local difference in Hedgehog signal transduction increases mechanical cell bond tension and biases cell intercalations along the Drosophila anteroposterior compartment boundary

et al. 2015

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Tissue organization requires the interplay between biochemical signaling and cellular force generation. The formation of straight boundaries separating cells with different fates into compartments is important for growth and patterning during tissue development. In the developing Drosophila wing disc, maintenance of the straight anteroposterior (AP) compartment boundary involves a local increase in mechanical tension at cell bonds along the boundary. The biochemical signals that regulate mechanical tension along the AP boundary, however, remain unknown. Here, we show that a local difference in Hedgehog signal transduction activity between anterior and posterior cells is necessary and sufficient to increase mechanical tension along the AP boundary. This difference in Hedgehog signal transduction is also required to bias cell rearrangements during cell intercalations to keep the characteristic straight shape of the AP boundary. Moreover, severing cell bonds along the AP boundary does not reduce tension at neighboring bonds, implying that active mechanical tension is upregulated, cell bond by cell bond. Finally, differences in the expression of the homeodomain-containing protein Engrailed also contribute to the straight shape of the AP boundary, independently of Hedgehog signal transduction and without modulating cell bond tension. Our data reveal a novel link between local differences in Hedgehog signal transduction and a local increase in active mechanical tension of cell bonds that biases junctional rearrangements. The large-scale shape of the AP boundary thus emerges from biochemical signals inducing patterns of active tension on cell bonds.

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Localization and requirement for Myosin II at the dorsal‐ventral compartment boundary of the Drosophila wing

Cited by 124 publications

References 44 publications

A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc

A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc

Cell rearrangements, cell divisions and cell death in a migrating epithelial sheet in the abdomen ofDrosophila

A local difference in Hedgehog signal transduction increases mechanical cell bond tension and biases cell intercalations along the Drosophila anteroposterior compartment boundary

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