Mechanical Signals Trigger Myosin II Redistribution and Mesoderm Invagination in Drosophila Embryos

Abstract

During Drosophila gastrulation, two waves of constriction occur in the apical ventral cells, leading to mesoderm invagination. The first constriction wave is a stochastic process mediated by the constriction of 40% of randomly positioned mesodermal cells and is controlled by the transcription factor Snail. The second constriction wave immediately follows and involves the other 60% of the mesodermal cells. The second wave is controlled by the transcription factor Twist and requires the secreted protein Fog. Complete mesoderm invagination requires redistribution of the motor protein Myosin II to the apical side of the constricting cells. We show that apical redistribution of Myosin II and mesoderm invagination, both of which are impaired in snail homozygous mutants that are defective in both constriction waves, are rescued by local mechanical deformation of the mesoderm with a micromanipulated needle. Mechanical deformation appears to promote Fog-dependent signaling by inhibiting Fog endocytosis. We propose that the mechanical tissue deformation that occurs during the Snail-dependent stochastic phase is necessary for the Fog-dependent signaling that mediates the second collective constriction wave.

Assessing the critical period for Rho kinase activity during Drosophila ventral furrow formation

“…Of interest, apical myosin II recruitment and VFF is rescued when a mechanical stimulus is applied to embryos ectopically expressing fog in either sna or sna, twi mutant embryos (Pouille et al, 2009). Without the mechanical stimulus, these embryos did not recruit myosin II, suggesting that an early mechanical strain driven by Fig.…”

“…The remainder developed normal appearing ventral furrows, but the ventral furrows were delayed or slow in forming. This may be attributed to the embryo's sensitivity to mechanical stress at this point in development (Pouille et al, 2009). …”

“…sna mutant embryos lack random and concerted apical constriction (Morize et al, 1998;Pouille et al, 2009). This may either indicate that Sna is required for both phases of apical constriction, or that concerted apical constriction is dependent on the proper initiation of random apical constriction.…”

“…This may either indicate that Sna is required for both phases of apical constriction, or that concerted apical constriction is dependent on the proper initiation of random apical constriction. twi mutant embryos have typical random apical constriction, but fail to develop concerted apical constrictions, thus random apical constriction phase appears to be Twiindependent while the concerted apical constriction phase requires Twi function (Costa et al, 1994;Ip et al, 1994;Dawes-Hoang et al, 2005;Martin et al, 2009;Pouille et al, 2009). A key downstream target of Twi is the secreted signaling protein, Fog.…”

“…[Color figure is available in the online issue, which is available at wileyonlinelibrary.com. ] sna expression is required to recruit myosin II apically (Pouille et al, 2009). Furthermore, embryos lacking Twi activity still undergo some shape changes, even though they do not form a ventral furrow.…”