JNK signaling coordinates integrin and actin functions during Drosophila embryogenesis

Abstract

Epithelial movements are key morphogenetic events in animal development. They are driven by multiple mechanisms, including signal-dependent changes in cytoskeletal organization and in cell adhesion. Such processes must be controlled precisely and coordinated to accurately sculpt the three-dimensional form of the developing organism. By observing the Drosophila epidermis during embryonic development using confocal time-lapse microscopy, we have investigated how signaling through the Jun-N-terminal kinase (JNK) pathway governs the tissue sheet movements that result in dorsal closure (DC). We find that JNK controls the polymerization of actin into a cable at the epidermal leading edge as previously suggested, as well as the joining (zipping) of the contralateral epithelial cell sheets. Here, we show that zipping is mediated by regulation of the integrins myospheroid and scab. Our data demonstrate that JNK signaling regulates a set of target genes that cooperate to facilitate epithelial movement and closure. Developmental Dynamics 235:427-434, 2006.

Actomyosin purse strings: Renewable resources that make morphogenesis robust and resilient

“…Note, these rates are indistinguishable from that of native closure in both our uncut control embryos (6.0± 0.8 nm/ s, n = 5) and our previously published, native embryos (Hutson et al, 2003;Homsy et al, 2006;Peralta et al, 2007). Following spaceship cuts, closure of the interrogated side of the embryo is delayed relative to the uncut side (43.3± 10.9 min, n =3).…”

Drosophilamorphogenesis: Tissue force laws and the modeling of dorsal closure

“…Native homozygous myospheroid mutant closure: Homozygous myospheroid mutant embryos are characterized by strong defects in zipping during native closure, followed by the failure of closure mediated primarily by the ripping apart of the boundary between the amnioserosa and the leading edge of the lateral epidermis, near the anterior end of the dorsal opening (Hutson et al, 2003;Homsy et al, 2006;Peralta et al, 2007). Other defects caused by mutations in integrin subunits or interacting proteins included delayed formation of the canthi and slowed closure, defects in adhesion between the amnioserosa and the yolk cell, defects in adhesion between the peripheral amnioserosa cells and the leading edge cells, aberrant actin rich purse strings, and alterations in the pattern of contraction of amnioserosa cells (Stark et al, 1997;Kadrmas et al, 2004;Narasimha and Brown, 2004;Reed et al, 2004;Wada et al, 2007;Gorfinkiel et al, 2009).…”

“…To investigate the forces responsible for the movements of closure described above, we and others have used a variety of laser microsurgery protocols and compared laserperturbed closure to native closure (Kiehart et al, 2000;Hutson et al, 2003;Homsy et al, 2006;Peralta et al, 2007Peralta et al, , 2008Rodriguez-Diaz et al, 2008;Thayil et al, 2008;Toyama et al, 2008;Solon et al, 2009). Here, closure is referred to as "native" when it is not laser-perturbed; thus, native closure can take place in wild-type or mutant embryos.…”

The Drosophila serine protease homologue Scarface regulates JNK signalling in a negative-feedback loop during epithelial morphogenesis

“…Precise activation of the JNK pathway, specifically in the dorsalmost row of epithelial cells in contact with the AS (the leading edge, LE), is a prerequisite for DC progression (Bates et al, 2008;Byars et al, 1999;Glise et al, 1995;Glise and Noselli, 1997;Martin-Blanco et al, 1998;Reed et al, 2001). Several transcriptional targets of the JNK pathway have already been described during DC, such as the profilin-coding gene chickadee, the transcription factor cabut, the integrin-coding genes scab and myospheroid or the trafficking gene Rab30 (Homsy et al, 2006;Jasper et al, 2001;Munoz-Descalzo et al, 2005;Thomas et al, 2009). However, only two target genes are specifically expressed in the LE, decapentaplegic (dpp) and puckered (puc) (Glise et al, 1995;Glise and Noselli, 1997).…”