Limits...
Regulating mechanical tension at compartment boundaries in Drosophila

View Article: PubMed Central - PubMed

ABSTRACT

During animal development, cells with similar function and fate often stay together and sort out from cells with different fates. In Drosophila wing imaginal discs, cells of anterior and posterior fates are separated by a straight compartment boundary. Separation of anterior and posterior cells requires the homeodomain-containing protein Engrailed, which is expressed in posterior cells. Engrailed induces the expression of the short-range signaling molecule Hedgehog in posterior cells and confines Hedgehog signal transduction to anterior cells. Transduction of the Hedgehog signal in anterior cells is required for the separation of anterior and posterior cells. Previous work showed that this separation of cells involves a local increase in mechanical tension at cell junctions along the compartment boundary. However, how mechanical tension was locally increased along the compartment boundary remained unknown. A recent paper now shows that the difference in Hedgehog signal transduction between anterior and posterior cells is necessary and sufficient to increase mechanical tension. The local increase in mechanical tension biases junctional rearrangements during cell intercalations to maintain the straight shape of the compartment boundary. These data highlight how developmental signals can generate patterns of mechanical tension important for tissue organization.

No MeSH data available.


Related in: MedlinePlus

Mechanisms by which Engrailed and Hedgehog contribute to the shaping of the AP boundary. (A) The selector gene engrailed is expressed in all cells of the posterior compartment and specifies posterior cell identity. (B) Engrailed induces the expression of the short-range signaling molecule Hedgehog (Hh). Hedgehog protein spreads to cells of the anterior compartment. Transduction of the Hedgehog signal requires the transmembrane protein Smoothened and leads to the activation of the transcription factor Ci, which induces the expression of Hedgehog target genes. Engrailed represses ci transcription in posterior cells. Thus, Engrailed results in a difference in Hedgehog signal transduction between anterior (ON) and posterior (OFF) cells. (C) The difference in Hedgehog signal transduction between anterior and posterior cells results in a local increase in mechanical tension (arrows) at cell bonds along the AP boundary. (D) The local increase in cell bond tension biases junctional rearrangements during cell intercalations along the AP boundary. (E) The bias in junctional rearrangements during cell intercalations contributes to the characteristic straight shape of the AP boundary. Engrailed, via a Hedgehog independent pathway, further contributes to the straight shape of the compartment boundary by an unknown mechanism.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC5036931&req=5

f0001: Mechanisms by which Engrailed and Hedgehog contribute to the shaping of the AP boundary. (A) The selector gene engrailed is expressed in all cells of the posterior compartment and specifies posterior cell identity. (B) Engrailed induces the expression of the short-range signaling molecule Hedgehog (Hh). Hedgehog protein spreads to cells of the anterior compartment. Transduction of the Hedgehog signal requires the transmembrane protein Smoothened and leads to the activation of the transcription factor Ci, which induces the expression of Hedgehog target genes. Engrailed represses ci transcription in posterior cells. Thus, Engrailed results in a difference in Hedgehog signal transduction between anterior (ON) and posterior (OFF) cells. (C) The difference in Hedgehog signal transduction between anterior and posterior cells results in a local increase in mechanical tension (arrows) at cell bonds along the AP boundary. (D) The local increase in cell bond tension biases junctional rearrangements during cell intercalations along the AP boundary. (E) The bias in junctional rearrangements during cell intercalations contributes to the characteristic straight shape of the AP boundary. Engrailed, via a Hedgehog independent pathway, further contributes to the straight shape of the compartment boundary by an unknown mechanism.

Mentions: The following model of how the AP boundary is established and maintained emerges (Fig. 1): The activity of the selector gene engrailed in posterior cells of wing imaginal discs has 2 functions in shaping the AP boundary: One function is independent of Hedgehog. The mechanism by which this function shapes the AP boundary is currently unknown. It apparently does not involve a local modulation of cell bond tension. The second function of Engrailed is to generate a difference in Hedgehog signal transduction activity between anterior (ON) and posterior (OFF) cells. This difference in Hedgehog signal transduction between anterior and posterior cells results in a local increase in cell bond tension along the AP boundary that in turn biases junctional rearrangements during cell intercalations to maintain the characteristic straight shape of the compartment boundary. The large-scale shape of the AP boundary is thus in part the result of a difference in Hedgehog signal transduction between anterior and posterior cells that induces a pattern of mechanical tension that in turn influences junctional rearrangements.Figure 1.


Regulating mechanical tension at compartment boundaries in Drosophila
Mechanisms by which Engrailed and Hedgehog contribute to the shaping of the AP boundary. (A) The selector gene engrailed is expressed in all cells of the posterior compartment and specifies posterior cell identity. (B) Engrailed induces the expression of the short-range signaling molecule Hedgehog (Hh). Hedgehog protein spreads to cells of the anterior compartment. Transduction of the Hedgehog signal requires the transmembrane protein Smoothened and leads to the activation of the transcription factor Ci, which induces the expression of Hedgehog target genes. Engrailed represses ci transcription in posterior cells. Thus, Engrailed results in a difference in Hedgehog signal transduction between anterior (ON) and posterior (OFF) cells. (C) The difference in Hedgehog signal transduction between anterior and posterior cells results in a local increase in mechanical tension (arrows) at cell bonds along the AP boundary. (D) The local increase in cell bond tension biases junctional rearrangements during cell intercalations along the AP boundary. (E) The bias in junctional rearrangements during cell intercalations contributes to the characteristic straight shape of the AP boundary. Engrailed, via a Hedgehog independent pathway, further contributes to the straight shape of the compartment boundary by an unknown mechanism.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5036931&req=5

f0001: Mechanisms by which Engrailed and Hedgehog contribute to the shaping of the AP boundary. (A) The selector gene engrailed is expressed in all cells of the posterior compartment and specifies posterior cell identity. (B) Engrailed induces the expression of the short-range signaling molecule Hedgehog (Hh). Hedgehog protein spreads to cells of the anterior compartment. Transduction of the Hedgehog signal requires the transmembrane protein Smoothened and leads to the activation of the transcription factor Ci, which induces the expression of Hedgehog target genes. Engrailed represses ci transcription in posterior cells. Thus, Engrailed results in a difference in Hedgehog signal transduction between anterior (ON) and posterior (OFF) cells. (C) The difference in Hedgehog signal transduction between anterior and posterior cells results in a local increase in mechanical tension (arrows) at cell bonds along the AP boundary. (D) The local increase in cell bond tension biases junctional rearrangements during cell intercalations along the AP boundary. (E) The bias in junctional rearrangements during cell intercalations contributes to the characteristic straight shape of the AP boundary. Engrailed, via a Hedgehog independent pathway, further contributes to the straight shape of the compartment boundary by an unknown mechanism.
Mentions: The following model of how the AP boundary is established and maintained emerges (Fig. 1): The activity of the selector gene engrailed in posterior cells of wing imaginal discs has 2 functions in shaping the AP boundary: One function is independent of Hedgehog. The mechanism by which this function shapes the AP boundary is currently unknown. It apparently does not involve a local modulation of cell bond tension. The second function of Engrailed is to generate a difference in Hedgehog signal transduction activity between anterior (ON) and posterior (OFF) cells. This difference in Hedgehog signal transduction between anterior and posterior cells results in a local increase in cell bond tension along the AP boundary that in turn biases junctional rearrangements during cell intercalations to maintain the characteristic straight shape of the compartment boundary. The large-scale shape of the AP boundary is thus in part the result of a difference in Hedgehog signal transduction between anterior and posterior cells that induces a pattern of mechanical tension that in turn influences junctional rearrangements.Figure 1.

View Article: PubMed Central - PubMed

ABSTRACT

During animal development, cells with similar function and fate often stay together and sort out from cells with different fates. In Drosophila wing imaginal discs, cells of anterior and posterior fates are separated by a straight compartment boundary. Separation of anterior and posterior cells requires the homeodomain-containing protein Engrailed, which is expressed in posterior cells. Engrailed induces the expression of the short-range signaling molecule Hedgehog in posterior cells and confines Hedgehog signal transduction to anterior cells. Transduction of the Hedgehog signal in anterior cells is required for the separation of anterior and posterior cells. Previous work showed that this separation of cells involves a local increase in mechanical tension at cell junctions along the compartment boundary. However, how mechanical tension was locally increased along the compartment boundary remained unknown. A recent paper now shows that the difference in Hedgehog signal transduction between anterior and posterior cells is necessary and sufficient to increase mechanical tension. The local increase in mechanical tension biases junctional rearrangements during cell intercalations to maintain the straight shape of the compartment boundary. These data highlight how developmental signals can generate patterns of mechanical tension important for tissue organization.

No MeSH data available.


Related in: MedlinePlus